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Central Circadian Clock Regulates Energy Metabolism

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Neural Regulation of Metabolism

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1090))

  • The original version of this chapter was revised: the funding information in the acknowledgements section was revised as requested by the authors. The correction to this chapter can be found at https://doi.org/10.1007/978-981-13-1286-1_13

Abstract

Our body not only responds to environmental changes but also anticipates them. The light and dark cycle with the period of about 24 h is a recurring environmental change that determines the diurnal variation in food availability and safety from predators in nature. As a result, the circadian clock is evolved in most animals to align locomotor behaviors and energy metabolism with the light cue. The central circadian clock in mammals is located at the suprachiasmatic nucleus (SCN) of the hypothalamus in the brain. We here review the molecular and anatomic architecture of the central circadian clock in mammals, describe the experimental and observational evidence that suggests a critical role of the central circadian clock in shaping systemic energy metabolism, and discuss the involvement of endocrine factors, neuropeptides, and the autonomic nervous system in the metabolic functions of the central circadian clock.

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Change history

  • 02 July 2019

    The below correction has been carried out in the page 93 of the current version

References

  1. Acosta-Galvan G, Yi C-X, van der Vliet J, Jhamandas JH, Panula P, Angeles-Castellanos M, Del Carmen Basualdo M, Escobar C, Buijs RM (2011) Interaction between hypothalamic dorsomedial nucleus and the suprachiasmatic nucleus determines intensity of food anticipatory behavior. Proc Natl Acad Sci U S A 108:5813–5818

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Agil A, Reiter RJ, Jiménez-Aranda A, Ibán-Arias R, Navarro-Alarcón M, Marchal JA, Adem A, Fernández-Vázquez G (2013) Melatonin ameliorates low-grade inflammation and oxidative stress in young Zucker diabetic fatty rats. J Pineal Res 54:381–388

    PubMed  Google Scholar 

  3. Albrecht U, Sun ZS, Eichele G, Lee CC (1997) A differential response of two putative mammalian circadian regulators, mper1 and mper2, to light. Cell 91:1055–1064

    CAS  PubMed  Google Scholar 

  4. Allison KC, Lundgren JD, O’Reardon JP, Geliebter A, Gluck ME, Vinai P, Mitchell JE, Schenck CH, Howell MJ, Crow SJ et al (2010) Proposed diagnostic criteria for night eating syndrome. Int J Eat Disord 43:241–247

    PubMed  PubMed Central  Google Scholar 

  5. An S, Harang R, Meeker K, Granados-Fuentes D, Tsai CA, Mazuski C, Kim J, Doyle FJ, Petzold LR, Herzog ED (2013) A neuropeptide speeds circadian entrainment by reducing intercellular synchrony. Proc Natl Acad Sci U S A 110:E4355–E4361

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Antunes LC, Levandovski R, Dantas G, Caumo W, Hidalgo MP (2010) Obesity and shift work: chronobiological aspects. Nutr Res Rev 23:155–168

    CAS  PubMed  Google Scholar 

  7. Arble DM, Holland J, Ottaway N, Sorrell J, Pressler JW, Morano R, Woods SC, Seeley RJ, Herman JP, Sandoval DA et al (2015) The melanocortin-4 receptor integrates circadian light cues and metabolism. Endocrinology 156:1685–1691

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Asensio C, Jimenez M, Kühne F, Rohner-Jeanrenaud F, Muzzin P (2005) The lack of beta-adrenoceptors results in enhanced insulin sensitivity in mice exhibiting increased adiposity and glucose intolerance. Diabetes 54:3490–3495

    CAS  PubMed  Google Scholar 

  9. 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 134:317–328

    CAS  PubMed  Google Scholar 

  10. Aubrecht TG, Jenkins R, Nelson RJ (2015) Dim light at night increases body mass of female mice. Chronobiol Int 32:557–560

    PubMed  Google Scholar 

  11. Balsalobre A, Damiola F, Schibler U (1998) A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93:929–937

    CAS  PubMed  Google Scholar 

  12. Barca-Mayo O, Pons-Espinal M, Follert P, Armirotti A, Berdondini L, De Pietri Tonelli D (2017) Astrocyte deletion of Bmal1 alters daily locomotor activity and cognitive functions via GABA signalling. Nat Commun 8:14336

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Bartness TJ, Song CK, Demas GE (2001) SCN efferents to peripheral tissues: implications for biological rhythms. J Biol Rhythm 16:196–204

    CAS  Google Scholar 

  14. Bedrosian TA, Fonken LK, Nelson RJ (2016) Endocrine effects of circadian disruption. Annu Rev Physiol 78:109–131

    CAS  PubMed  Google Scholar 

  15. Belle MDC, Hughes ATL, Bechtold DA, Cunningham P, Pierucci M, Burdakov D, Piggins HD (2014) Acute suppressive and long-term phase modulation actions of orexin on the mammalian circadian clock. J Neurosci 34:3607–3621

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Below JE, Gamazon ER, Morrison JV, Konkashbaev A, Pluzhnikov A, McKeigue PM, Parra EJ, Elbein SC, Hallman DM, Nicolae DL et al (2011) Genome-wide association and meta-analysis in populations from Starr County, Texas, and Mexico City identify type 2 diabetes susceptibility loci and enrichment for expression quantitative trait loci in top signals. Diabetologia 54:2047–2055

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Bonnefond A, Froguel P (2017) Disentangling the role of melatonin and its receptor MTNR1B in type 2 diabetes: still a long way to go? Curr Diab Rep 17:122

    PubMed  Google Scholar 

  18. Bouatia-Naji N, Bonnefond A, Cavalcanti-Proença C, Sparsø T, Holmkvist J, Marchand M, Delplanque J, Lobbens S, Rocheleau G, Durand E et al (2009) A variant near MTNR1B is associated with increased fasting plasma glucose levels and type 2 diabetes risk. Nat Genet 41:89–94

    CAS  PubMed  Google Scholar 

  19. Brancaccio M, Patton AP, Chesham JE, Maywood ES, Hastings MH (2017) Astrocytes control circadian timekeeping in the suprachiasmatic nucleus via glutamatergic signaling. Neuron 93:1420–1435.e5

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Bray MS, Tsai J-Y, Villegas-Montoya C, Boland BB, Blasier Z, Egbejimi O, Kueht M, Young ME (2010) Time-of-day-dependent dietary fat consumption influences multiple cardiometabolic syndrome parameters in mice. Int J Obes 2005(34):1589–1598

    Google Scholar 

  21. Bray MS, Ratcliffe WF, Grenett MH, Brewer RA, Gamble KL, Young ME (2013) Quantitative analysis of light-phase restricted feeding reveals metabolic dyssynchrony in mice. Int J Obes 2005(37):843–852

    Google Scholar 

  22. Buijs RM, Kalsbeek A (2001) Hypothalamic integration of central and peripheral clocks. Nat Rev Neurosci 2:521–526

    CAS  PubMed  Google Scholar 

  23. Buijs RM, Hermes MH, Kalsbeek A (1998) The suprachiasmatic nucleus-paraventricular nucleus interactions: a bridge to the neuroendocrine and autonomic nervous system. Prog Brain Res 119:365–382

    CAS  PubMed  Google Scholar 

  24. Buijs FN, Guzmán-Ruiz M, León-Mercado L, Basualdo MC, Escobar C, Kalsbeek A, Buijs RM (2017) suprachiasmatic nucleus interaction with the arcuate nucleus; essential for organizing physiological rhythms. ENeuro 4

    Google Scholar 

  25. Bunger MK, Wilsbacher LD, Moran SM, Clendenin C, Radcliffe LA, Hogenesch JB, Simon MC, Takahashi JS, Bradfield CA (2000) Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103:1009–1017

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Burcelin R, Uldry M, Foretz M, Perrin C, Dacosta A, Nenniger-Tosato M, Seydoux J, Cotecchia S, Thorens B (2004) Impaired glucose homeostasis in mice lacking the alpha1b-adrenergic receptor subtype. J Biol Chem 279:1108–1115

    CAS  PubMed  Google Scholar 

  27. Busino L, Bassermann F, Maiolica A, Lee C, Nolan PM, Godinho SIH, Draetta GF, Pagano M (2007) SCFFbxl3 controls the oscillation of the circadian clock by directing the degradation of cryptochrome proteins. Science 316:900–904

    CAS  PubMed  Google Scholar 

  28. Cagnacci A, Arangino S, Renzi A, Paoletti AM, Melis GB, Cagnacci P, Volpe A (2001) Influence of melatonin administration on glucose tolerance and insulin sensitivity of postmenopausal women. Clin Endocrinol 54:339–346

    CAS  Google Scholar 

  29. Cailotto C, La Fleur SE, Van Heijningen C, Wortel J, Kalsbeek A, Feenstra M, Pévet P, Buijs RM (2005) The suprachiasmatic nucleus controls the daily variation of plasma glucose via the autonomic output to the liver: are the clock genes involved? Eur J Neurosci 22:2531–2540

    PubMed  Google Scholar 

  30. Cailotto C, van Heijningen C, van der Vliet J, van der Plasse G, Habold C, Kalsbeek A, Pévet P, Buijs RM (2008) Daily rhythms in metabolic liver enzymes and plasma glucose require a balance in the autonomic output to the liver. Endocrinology 149:1914–1925

    CAS  PubMed  Google Scholar 

  31. Cedernaes J, Lampola L, Axelsson EK, Liethof L, Hassanzadeh S, Yeganeh A, Broman J-E, Schiöth HB, Benedict C (2016) A single night of partial sleep loss impairs fasting insulin sensitivity but does not affect cephalic phase insulin release in young men. J Sleep Res 25:5–10

    PubMed  Google Scholar 

  32. Challet E (2007) Minireview: Entrainment of the suprachiasmatic clockwork in diurnal and nocturnal mammals. Endocrinology 148:5648–5655

    CAS  PubMed  Google Scholar 

  33. Challet E, Malan A, Turek FW, Van Reeth O (2004) Daily variations of blood glucose, acid-base state and PCO2 in rats: effect of light exposure. Neurosci Lett 355:131–135

    CAS  PubMed  Google Scholar 

  34. Chemelli RM, Willie JT, Sinton CM, Elmquist JK, Scammell T, Lee C, Richardson JA, Williams SC, Xiong Y, Kisanuki Y et al (1999) Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 98:437–451

    CAS  PubMed  Google Scholar 

  35. Chen L, Mullegama SV, Alaimo JT, Elsea SH (2015) Smith-Magenis syndrome and its circadian influence on development, behavior, and obesity – own experience. Dev Period Med 19:149–156

    PubMed  Google Scholar 

  36. Chieffi S, Carotenuto M, Monda V, Valenzano A, Villano I, Precenzano F, Tafuri D, Salerno M, Filippi N, Nuccio F et al (2017) Orexin system: the key for a healthy life. Front Physiol 8:357

    PubMed  PubMed Central  Google Scholar 

  37. Coomans CP, van den Berg SAA, Houben T, van Klinken J-B, van den Berg R, Pronk ACM, Havekes LM, Romijn JA, van Dijk KW, Biermasz NR et al (2013a) Detrimental effects of constant light exposure and high-fat diet on circadian energy metabolism and insulin sensitivity. FASEB J Off Publ Fed Am Soc Exp Biol 27:1721–1732

    CAS  Google Scholar 

  38. Coomans CP, van den Berg SAA, Lucassen EA, Houben T, Pronk ACM, van der Spek RD, Kalsbeek A, Biermasz NR, Willems van Dijk K, Romijn JA et al (2013b) The suprachiasmatic nucleus controls circadian energy metabolism and hepatic insulin sensitivity. Diabetes 62:1102–1108

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Curtis AM, Seo S, Westgate EJ, Rudic RD, Smyth EM, Chakravarti D, FitzGerald GA, McNamara P (2004) Histone acetyltransferase-dependent chromatin remodeling and the vascular clock. J Biol Chem 279:7091–7097

    CAS  PubMed  Google Scholar 

  40. Dardente H, Menet JS, Challet E, Tournier BB, Pévet P, Masson-Pévet M (2004) Daily and circadian expression of neuropeptides in the suprachiasmatic nuclei of nocturnal and diurnal rodents. Brain Res Mol Brain Res 124:143–151

    CAS  PubMed  Google Scholar 

  41. DeBruyne JP, Weaver DR, Reppert SM (2007) CLOCK and NPAS2 have overlapping roles in the suprachiasmatic circadian clock. Nat Neurosci 10:543–545

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Diabetes Genetics Initiative of Broad Institute of Harvard and MIT, Lund University, and Novartis Institutes of Bio Medical Research, Saxena R, Voight BF, Lyssenko V, Burtt NP, de Bakker PIW, Chen H, Roix JJ, Kathiresan S, Hirschhorn JN et al (2007) Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science 316:1331–1336

    Google Scholar 

  43. DiTacchio L, Le HD, Vollmers C, Hatori M, Witcher M, Secombe J, Panda S (2011) Histone lysine demethylase JARID1a activates CLOCK-BMAL1 and influences the circadian clock. Science 333:1881–1885

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Doi M, Hirayama J, Sassone-Corsi P (2006) Circadian regulator CLOCK is a histone acetyltransferase. Cell 125:497–508

    CAS  PubMed  Google Scholar 

  45. Dumas B, Harding HP, Choi HS, Lehmann KA, Chung M, Lazar MA, Moore DD (1994) A new orphan member of the nuclear hormone receptor superfamily closely related to Rev-Erb. Mol Endocrinol Baltim Md 8:996–1005

    CAS  Google Scholar 

  46. Duong HA, Weitz CJ (2014) Temporal orchestration of repressive chromatin modifiers by circadian clock period complexes. Nat Struct Mol Biol 21:126–132

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Dupuis J, Langenberg C, Prokopenko I, Saxena R, Soranzo N, Jackson AU, Wheeler E, Glazer NL, Bouatia-Naji N, Gloyn AL et al (2010) New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk. Nat Genet 42:105–116

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Eckel RH, Depner CM, Perreault L, Markwald RR, Smith MR, McHill AW, Higgins J, Melanson EL, Wright KP (2015) Morning circadian misalignment during short sleep duration impacts insulin sensitivity. Curr Biol CB 25:3004–3010

    CAS  PubMed  Google Scholar 

  49. Eckel-Mahan K, Sassone-Corsi P (2013) Metabolism and the circadian clock converge. Physiol Rev 93:107–135

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Eckel-Mahan KL, Patel VR, de Mateo S, Orozco-Solis R, Ceglia NJ, Sahar S, Dilag-Penilla SA, Dyar KA, Baldi P, Sassone-Corsi P (2013) Reprogramming of the circadian clock by nutritional challenge. Cell 155:1464–1478

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Edgar DM, Reid MS, Dement WC (1997) Serotonergic afferents mediate activity-dependent entrainment of the mouse circadian clock. Am J Phys 273:R265–R269

    CAS  Google Scholar 

  52. Etchegaray J-P, Lee C, Wade PA, Reppert SM (2003) Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature 421:177–182

    CAS  PubMed  Google Scholar 

  53. Etchegaray J-P, Yang X, DeBruyne JP, Peters AHFM, Weaver DR, Jenuwein T, Reppert SM (2006) The polycomb group protein EZH2 is required for mammalian circadian clock function. J Biol Chem 281:21209–21215

    CAS  PubMed  Google Scholar 

  54. Fagerholm V, Grönroos T, Marjamäki P, Viljanen T, Scheinin M, Haaparanta M (2004) Altered glucose homeostasis in alpha2A-adrenoceptor knockout mice. Eur J Pharmacol 505:243–252

    CAS  PubMed  Google Scholar 

  55. Feng D, Liu T, Sun Z, Bugge A, Mullican SE, Alenghat T, Liu XS, Lazar MA (2011) A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism. Science 331:1315–1319

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Fernandes GW, Ueta CB, Fonseca TL, Gouveia CHA, Lancellotti CL, Brum PC, Christoffolete MA, Bianco AC, Ribeiro MO (2014) Inactivation of the adrenergic receptor β2 disrupts glucose homeostasis in mice. J Endocrinol 221:381–390

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Fonken L, Nelson R (2014) The effects of light at night on circadian clocks and metabolism. Endocr Rev. 35(4):648–670.

    CAS  PubMed  Google Scholar 

  58. Foppen E, Tan AAT, Ackermans MT, Fliers E, Kalsbeek A (2016) Suprachiasmatic Nucleus Neuropeptides and Their Control of Endogenous Glucose Production. J Neuroendocrinol 28

    Google Scholar 

  59. Forrestel AC, Miedlich SU, Yurcheshen M, Wittlin SD, Sellix MT (2017) Chronomedicine and type 2 diabetes: shining some light on melatonin. Diabetologia 60:808–822

    CAS  PubMed  Google Scholar 

  60. Gachon F, Fonjallaz P, Damiola F, Gos P, Kodama T, Zakany J, Duboule D, Petit B, Tafti M, Schibler U (2004) The loss of circadian PAR bZip transcription factors results in epilepsy. Genes Dev 18:1397–1412

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Gallant AR, Lundgren J, Drapeau V (2012) The night-eating syndrome and obesity. Obes Rev Off J Int Assoc Study Obes 13:528–536

    CAS  Google Scholar 

  62. Gamble KL, Berry R, Frank SJ, Young ME (2014) Circadian clock control of endocrine factors. Nat Rev Endocrinol 10:466–475

    PubMed  PubMed Central  Google Scholar 

  63. Gekakis N, Staknis D, Nguyen HB, Davis FC, Wilsbacher LD, King DP, Takahashi JS, Weitz CJ (1998) Role of the CLOCK protein in the mammalian circadian mechanism. Science 280:1564–1569

    CAS  PubMed  Google Scholar 

  64. Godinho SIH, Maywood ES, Shaw L, Tucci V, Barnard AR, Busino L, Pagano M, Kendall R, Quwailid MM, Romero MR et al (2007) The after-hours mutant reveals a role for Fbxl3 in determining mammalian circadian period. Science 316:897–900

    CAS  PubMed  Google Scholar 

  65. Guo H, Brewer JM, Champhekar A, Harris RBS, Bittman EL (2005) Differential control of peripheral circadian rhythms by suprachiasmatic-dependent neural signals. Proc Natl Acad Sci U S A 102:3111–3116

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Guzmán-Ruiz M, Saderi N, Cazarez-Márquez F, Guerrero-Vargas NN, Basualdo MC, Acosta-Galván G, Buijs RM (2014) The suprachiasmatic nucleus changes the daily activity of the arcuate nucleus α-MSH neurons in male rats. Endocrinology 155:525–535

    PubMed  Google Scholar 

  67. Guzmán-Ruiz MA, Ramirez-Corona A, Guerrero-Vargas NN, Sabath E, Ramirez-Plascencia OD, Fuentes-Romero R, León-Mercado LA, Basualdo Sigales M, Escobar C, Buijs RM (2015) Role of the suprachiasmatic and arcuate nuclei in diurnal temperature regulation in the rat. J Neurosci 35:15419–15429

    PubMed  Google Scholar 

  68. Hamaguchi Y, Tahara Y, Hitosugi M, Shibata S (2015) Impairment of circadian rhythms in peripheral clocks by constant light is partially reversed by scheduled feeding or exercise. J Biol Rhythm 30:533–542

    CAS  Google Scholar 

  69. Hanna L, Walmsley L, Pienaar A, Howarth M, Brown TM (2017) Geniculohypothalamic GABAergic projections gate suprachiasmatic nucleus responses to retinal input. J Physiol 595:3621–3649

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Hara J, Yanagisawa M, Sakurai T (2005) Difference in obesity phenotype between orexin-knockout mice and orexin neuron-deficient mice with same genetic background and environmental conditions. Neurosci Lett 380:239–242

    CAS  PubMed  Google Scholar 

  71. Harrington ME (1997) The ventral lateral geniculate nucleus and the intergeniculate leaflet: interrelated structures in the visual and circadian systems. Neurosci Biobehav Rev 21:705–727

    CAS  PubMed  Google Scholar 

  72. Hatori M, Vollmers C, Zarrinpar A, DiTacchio L, Bushong EA, Gill S, Leblanc M, Chaix A, Joens M, Fitzpatrick JAJ et al (2012) Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab 15:848–860

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Hong S, Zhou W, Fang B, Lu W, Loro E, Damle M, Ding G, Jager J, Zhang S, Zhang Y et al (2017) Dissociation of muscle insulin sensitivity from exercise endurance in mice by HDAC3 depletion. Nat Med 23:223–234

    CAS  PubMed  Google Scholar 

  74. Hut RA, Kronfeld-Schor N, van der Vinne V, De la Iglesia H (2012) In search of a temporal niche: environmental factors. Prog Brain Res 199:281–304

    PubMed  Google Scholar 

  75. Ibuka N, Inouye SI, Kawamura H (1977) Analysis of sleep-wakefulness rhythms in male rats after suprachiasmatic nucleus lesions and ocular enucleation. Brain Res 122:33–47

    CAS  PubMed  Google Scholar 

  76. Kaasik K, Kivimäe S, Allen JJ, Chalkley RJ, Huang Y, Baer K, Kissel H, Burlingame AL, Shokat KM, Ptáček LJ et al (2013) Glucose sensor O-GlcNAcylation coordinates with phosphorylation to regulate circadian clock. Cell Metab 17:291–302

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Kalsbeek A, Fliers E (2013) Daily regulation of hormone profiles. Handb Exp Pharmacol 217:185–226

    CAS  Google Scholar 

  78. Kalsbeek A, Strubbe JH (1998) Circadian control of insulin secretion is independent of the temporal distribution of feeding. 63(4):553–558.

    Google Scholar 

  79. 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 24:7604–7613

    CAS  PubMed  Google Scholar 

  80. Kalsbeek A, Foppen E, Schalij I, Van Heijningen C, van der Vliet J, Fliers E, Buijs RM (2008a) Circadian control of the daily plasma glucose rhythm: an interplay of GABA and glutamate. PloS One 3:e3194

    PubMed  PubMed Central  Google Scholar 

  81. Kalsbeek A, Verhagen LAW, Schalij I, Foppen E, Saboureau M, Bothorel B, Buijs RM, Pévet P (2008b) Opposite actions of hypothalamic vasopressin on circadian corticosterone rhythm in nocturnal versus diurnal species. Eur J Neurosci 27:818–827

    PubMed  Google Scholar 

  82. Kalsbeek A, la Fleur S, Fliers E (2014) Circadian control of glucose metabolism. Mol Metab 3:372–383

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Karlsson B, Knutsson A, Lindahl B (2001) Is there an association between shift work and having a metabolic syndrome? Results from a population based study of 27,485 people. Occup Environ Med 58:747–752

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Kasahara T, Abe K, Mekada K, Yoshiki A, Kato T (2010) Genetic variation of melatonin productivity in laboratory mice under domestication. Proc Natl Acad Sci U S A 107:6412–6417

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Katada S, Sassone-Corsi P (2010) The histone methyltransferase MLL1 permits the oscillation of circadian gene expression. Nat Struct Mol Biol 17:1414–1421

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Kitazawa M (2013) Circadian rhythms, metabolism, and insulin sensitivity: transcriptional networks in animal models. Curr Diab Rep 13:223–228

    CAS  PubMed  Google Scholar 

  87. Kooijman S, van den Berg R, Ramkisoensing A, Boon MR, Kuipers EN, Loef M, Zonneveld TCM, Lucassen EA, Sips HCM, Chatzispyrou IA et al (2015) Prolonged daily light exposure increases body fat mass through attenuation of brown adipose tissue activity. Proc Natl Acad Sci U S A 112:6748–6753

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Koren D, Dumin M, Gozal D (2016) Role of sleep quality in the metabolic syndrome. Diabetes Metab Syndr Obes Targets Ther 9:281–310

    CAS  Google Scholar 

  89. Kubo T, Oyama I, Nakamura T, Shirane K, Otsuka H, Kunimoto M, Kadowaki K, Maruyama T, Otomo H, Fujino Y et al (2011) Retrospective cohort study of the risk of obesity among shift workers: findings from the Industry-based Shift Workers’ Health study, Japan. Occup Environ Med 68:327–331

    PubMed  Google Scholar 

  90. Kume K, Zylka MJ, Sriram S, Shearman LP, Weaver DR, Jin X, Maywood ES, Hastings MH, Reppert SM (1999) mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98:193–205

    CAS  PubMed  Google Scholar 

  91. La Fleur SE (2003) Daily rhythms in glucose metabolism: suprachiasmatic nucleus output to peripheral tissue. J Neuroendocrinol 15:315–322

    PubMed  Google Scholar 

  92. La Fleur SE, Kalsbeek A, Wortel J, Buijs RM (1999) A suprachiasmatic nucleus generated rhythm in basal glucose concentrations. J Neuroendocrinol 11:643–652

    PubMed  Google Scholar 

  93. la Fleur SE, Kalsbeek A, Wortel J, Fekkes ML, Buijs RM (2001a) A daily rhythm in glucose tolerance: a role for the suprachiasmatic nucleus. Diabetes 50:1237–1243

    PubMed  Google Scholar 

  94. la Fleur SE, Kalsbeek A, Wortel J, van der Vliet J, Buijs RM (2001b) Role for the pineal and melatonin in glucose homeostasis: pinealectomy increases night-time glucose concentrations. J Neuroendocrinol 13:1025–1032

    PubMed  Google Scholar 

  95. Lamia KA, Sachdeva UM, DiTacchio L, Williams EC, Alvarez JG, Egan DF, Vasquez DS, Juguilon H, Panda S, Shaw RJ et al (2009) AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science 326:437–440

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Lazar MA, Hodin RA, Chin WW (1989) Human carboxyl-terminal variant of alpha-type c-erbA inhibits trans-activation by thyroid hormone receptors without binding thyroid hormone. Proc Natl Acad Sci U S A 86:7771–7774

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Leak RK, Moore RY (2001) Topographic organization of suprachiasmatic nucleus projection neurons. J Comp Neurol 433:312–334

    CAS  PubMed  Google Scholar 

  98. Leak RK, Card JP, Moore RY (1999) Suprachiasmatic pacemaker organization analyzed by viral transynaptic transport. Brain Res 819:23–32

    CAS  PubMed  Google Scholar 

  99. Lee H, Chen R, Kim H, Etchegaray J-P, Weaver DR, Lee C (2011) The period of the circadian oscillator is primarily determined by the balance between casein kinase 1 and protein phosphatase 1. Proc Natl Acad Sci U S A 108:16451–16456

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Lehman MN, Silver R, Gladstone WR, Kahn RM, Gibson M, Bittman EL (1987) Circadian rhythmicity restored by neural transplant. Immunocytochemical characterization of the graft and its integration with the host brain. J Neurosci 7:1626–1638

    CAS  PubMed  Google Scholar 

  101. LeSauter J, Romero P, Cascio M, Silver R (1997) Attachment site of grafted SCN influences precision of restored circadian rhythm. J Biol Rhythm 12:327–338

    CAS  Google Scholar 

  102. Leung GKW, Huggins CE, Bonham MP (2017) Effect of meal timing on postprandial glucose responses to a low glycemic index meal: a crossover trial in healthy volunteers. Clin Nutr Edinb Scotl

    Google Scholar 

  103. Li JH, Gautam D, Han S-J, Guettier J-M, Cui Y, Lu H, Deng C, O’Hare J, Jou W, Gavrilova O et al (2009) Hepatic muscarinic acetylcholine receptors are not critically involved in maintaining glucose homeostasis in mice. Diabetes 58:2776–2787

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Lin L, Faraco J, Li R, Kadotani H, Rogers W, Lin X, Qiu X, de Jong PJ, Nishino S, Mignot E (1999) The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell 98:365–376

    CAS  PubMed  Google Scholar 

  105. Lu J, Zhang YH, Chou TC, Gaus SE, Elmquist JK, Shiromani P, Saper CB (2001) Contrasting effects of ibotenate lesions of the paraventricular nucleus and subparaventricular zone on sleep-wake cycle and temperature regulation. J Neurosci 21:4864–4874

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Lucas RJ, Lall GS, Allen AE, Brown TM (2012) How rod, cone, and melanopsin photoreceptors come together to enlighten the mammalian circadian clock. Prog Brain Res 199:1–18

    CAS  PubMed  Google Scholar 

  107. Lyssenko V, Nagorny CLF, Erdos MR, Wierup N, Jonsson A, Spégel P, Bugliani M, Saxena R, Fex M, Pulizzi N et al (2009) Common variant in MTNR1B associated with increased risk of type 2 diabetes and impaired early insulin secretion. Nat Genet 41:82–88

    CAS  PubMed  Google Scholar 

  108. Malloy JN, Paulose JK, Li Y, Cassone VM (2012) Circadian rhythms of gastrointestinal function are regulated by both central and peripheral oscillators. Am J Physiol Gastrointest Liver Physiol 303:G461–G473

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Marcheva B, Ramsey KM, Buhr ED, Kobayashi Y, Su H, Ko CH, Ivanova G, Omura C, Mo S, Vitaterna MH et al (2010) Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 466:627–631

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Marston OJ, Williams RH, Canal MM, Samuels RE, Upton N, Piggins HD (2008) Circadian and dark-pulse activation of orexin/hypocretin neurons. Mol Brain 1:19

    PubMed  PubMed Central  Google Scholar 

  111. Mendoza-Viveros L, Bouchard-Cannon P, Hegazi S, Cheng AH, Pastore S, Cheng H-YM (2017) Molecular modulators of the circadian clock: lessons from flies and mice. Cell Mol Life Sci CMLS 74:1035–1059

    CAS  PubMed  Google Scholar 

  112. Meyer-Bernstein EL, Jetton AE, Matsumoto SI, Markuns JF, Lehman MN, Bittman EL (1999) Effects of suprachiasmatic transplants on circadian rhythms of neuroendocrine function in golden hamsters. Endocrinology 140:207–218

    CAS  PubMed  Google Scholar 

  113. Mikkelsen JD (1992) The organization of the crossed geniculogeniculate pathway of the rat: a Phaseolus vulgaris-leucoagglutinin study. Neuroscience 48:953–962

    CAS  PubMed  Google Scholar 

  114. Mistlberger RE, Antle MC, Glass JD, Miller JD (2000) Behavioral and Serotonergic Regulation of Circadian Rhythms. Biol Rhythm Res 31:240–283

    CAS  Google Scholar 

  115. Mitsui S, Yamaguchi S, Matsuo T, Ishida Y, Okamura H (2001) Antagonistic role of E4BP4 and PAR proteins in the circadian oscillatory mechanism. Genes Dev 15:995–1006

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Miyajima N, Horiuchi R, Shibuya Y, Fukushige S, Matsubara K, Toyoshima K, Yamamoto T (1989) Two erbA homologs encoding proteins with different T3 binding capacities are transcribed from opposite DNA strands of the same genetic locus. Cell 57:31–39

    CAS  PubMed  Google Scholar 

  117. Monnier L, Colette C, Dejager S, Owens D (2013) Magnitude of the dawn phenomenon and its impact on the overall glucose exposure in type 2 diabetes: is this of concern? Diabetes Care 36:4057–4062

    CAS  PubMed  PubMed Central  Google Scholar 

  118. Moore RY, Weis R, Moga MM (2000) Efferent projections of the intergeniculate leaflet and the ventral lateral geniculate nucleus in the rat. J Comp Neurol 420:398–418

    CAS  PubMed  Google Scholar 

  119. Morin LP (1999) Serotonin and the regulation of mammalian circadian rhythmicity. Ann Med 31:12–33

    CAS  PubMed  Google Scholar 

  120. Morin LP (2013) Neuroanatomy of the extended circadian rhythm system. Exp Neurol 243:4–20

    PubMed  Google Scholar 

  121. Nagai K, Nagai N, Sugahara K, Niijima A, Nakagawa H (1994) Circadian rhythms and energy metabolism with special reference to the suprachiasmatic nucleus. Neurosci Biobehav Rev 18:579–584

    CAS  PubMed  Google Scholar 

  122. 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 134:329–340

    CAS  PubMed  PubMed Central  Google Scholar 

  123. Nduhirabandi F, Du Toit EF, Blackhurst D, Marais D, Lochner A (2011) Chronic melatonin consumption prevents obesity-related metabolic abnormalities and protects the heart against myocardial ischemia and reperfusion injury in a prediabetic model of diet-induced obesity. J Pineal Res 50:171–182

    CAS  PubMed  Google Scholar 

  124. O’Reardon JP, Stunkard AJ, Allison KC (2004) Clinical trial of sertraline in the treatment of night eating syndrome. Int J Eat Disord 35:16–26

    PubMed  Google Scholar 

  125. Opperhuizen A-L, van Kerkhof LWM, Proper KI, Rodenburg W, Kalsbeek A (2015) Rodent models to study the metabolic effects of shiftwork in humans. Front Pharmacol 6:50

    PubMed  PubMed Central  Google Scholar 

  126. Orozco-Solis R, Aguilar-Arnal L, Murakami M, Peruquetti R, Ramadori G, Coppari R, Sassone-Corsi P (2016) The circadian clock in the ventromedial hypothalamus controls cyclic energy expenditure. Cell Metab 23:467–478

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Oster H, Challet E, Ott V, Arvat E, de Kloet ER, Dijk D-J, Lightman S, Vgontzas A, Van Cauter E (2017) The functional and clinical significance of the 24-hour rhythm of circulating glucocorticoids. Endocr Rev 38:3–45

    PubMed  Google Scholar 

  128. Owino S, Contreras-Alcantara S, Baba K, Tosini G (2016) Melatonin signaling controls the daily rhythm in blood glucose levels independent of peripheral clocks. PloS One 11:e0148214

    PubMed  PubMed Central  Google Scholar 

  129. Palus K, Chrobok L, Lewandowski MH (2015) Orexins/hypocretins modulate the activity of NPY-positive and -negative neurons in the rat intergeniculate leaflet via OX1 and OX2 receptors. Neuroscience 300:370–380

    CAS  PubMed  Google Scholar 

  130. Peterhoff M, Sieg A, Brede M, Chao C-M, Hein L, Ullrich S (2003) Inhibition of insulin secretion via distinct signaling pathways in alpha2-adrenoceptor knockout mice. Eur J Endocrinol 149:343–350

    CAS  PubMed  Google Scholar 

  131. Pezük P, Mohawk JA, Wang LA, Menaker M (2012) Glucocorticoids as entraining signals for peripheral circadian oscillators. Endocrinology 153:4775–4783

    PubMed  PubMed Central  Google Scholar 

  132. Pickard GE (1982) The afferent connections of the suprachiasmatic nucleus of the golden hamster with emphasis on the retinohypothalamic projection. J Comp Neurol 211:65–83

    CAS  PubMed  Google Scholar 

  133. Preite NZ, do Nascimento BPP, Muller CR, Américo ALV, Higa TS, Evangelista FS, Lancellotti CL, Henriques F d S, Batista ML, Bianco AC et al (2016) Disruption of beta3 adrenergic receptor increases susceptibility to DIO in mouse. J Endocrinol 231:259–269

    CAS  PubMed  PubMed Central  Google Scholar 

  134. Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, Albrecht U, 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

    CAS  PubMed  Google Scholar 

  135. Prokopenko I, Langenberg C, Florez JC, Saxena R, Soranzo N, Thorleifsson G, Loos RJF, Manning AK, Jackson AU, Aulchenko Y et al (2009) Variants in MTNR1B influence fasting glucose levels. Nat Genet 41:77–81

    CAS  PubMed  Google Scholar 

  136. Ralph MR, Foster RG, Davis FC, Menaker M (1990) Transplanted suprachiasmatic nucleus determines circadian period. Science 247:975–978

    CAS  PubMed  Google Scholar 

  137. Rao MN, Neylan TC, Grunfeld C, Mulligan K, Schambelan M, Schwarz J-M (2015) Subchronic sleep restriction causes tissue-specific insulin resistance. J Clin Endocrinol Metab 100:1664–1671

    CAS  PubMed  PubMed Central  Google Scholar 

  138. 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. Hepatol Baltim Md 45:1478–1488

    CAS  Google Scholar 

  139. Reghunandanan V, Reghunandanan R (2006) Neurotransmitters of the suprachiasmatic nuclei. J Circadian Rhythms 4:2

    PubMed  PubMed Central  Google Scholar 

  140. Roenneberg T, Merrow M (2016) The circadian clock and human health. Curr Biol CB 26:R432–R443

    CAS  PubMed  Google Scholar 

  141. Roseboom PH, Namboodiri MA, Zimonjic DB, Popescu NC, Rodriguez IR, Gastel JA, Klein DC (1998) Natural melatonin “knockdown” in C57BL/6J mice: rare mechanism truncates serotonin N-acetyltransferase. Brain Res Mol Brain Res 63:189–197

    CAS  PubMed  Google Scholar 

  142. Rubio-Sastre P, Scheer FAJL, Gómez-Abellán P, Madrid JA, Garaulet M (2014) Acute melatonin administration in humans impairs glucose tolerance in both the morning and evening. Sleep 37:1715–1719

    PubMed  PubMed Central  Google Scholar 

  143. Ruohonen ST, Ruohonen S, Gilsbach R, Savontaus E, Scheinin M, Hein L (2012) Involvement of α2-adrenoceptor subtypes A and C in glucose homeostasis and adrenaline-induced hyperglycaemia. Neuroendocrinology 96:51–59

    CAS  PubMed  Google Scholar 

  144. Sato TK, Panda S, Miraglia LJ, Reyes TM, Rudic RD, McNamara P, Naik KA, FitzGerald GA, Kay SA, Hogenesch JB (2004) A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron 43:527–537

    CAS  PubMed  Google Scholar 

  145. Savontaus E, Fagerholm V, Rahkonen O, Scheinin M (2008) Reduced blood glucose levels, increased insulin levels and improved glucose tolerance in alpha2A-adrenoceptor knockout mice. Eur J Pharmacol 578:359–364

    CAS  PubMed  Google Scholar 

  146. Schwartz MD, Urbanski HF, Nunez AA, Smale L (2011) Projections of the suprachiasmatic nucleus and ventral subparaventricular zone in the Nile grass rat (Arvicanthis niloticus). Brain Res 1367:146–161

    CAS  PubMed  Google Scholar 

  147. Scott LJ, Mohlke KL, Bonnycastle LL, Willer CJ, Li Y, Duren WL, Erdos MR, Stringham HM, Chines PS, Jackson AU et al (2007) A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science 316:1341–1345

    CAS  PubMed  PubMed Central  Google Scholar 

  148. Scott EM, Carter AM, Grant PJ (2008) Association between polymorphisms in the Clock gene, obesity and the metabolic syndrome in man. Int J Obes 2005(32):658–662

    Google Scholar 

  149. Shearman LP, Zylka MJ, Weaver DR, Kolakowski LF, Reppert SM (1997) Two period homologs: circadian expression and photic regulation in the suprachiasmatic nuclei. Neuron 19:1261–1269

    CAS  PubMed  Google Scholar 

  150. Shearman LP, Sriram S, Weaver DR, Maywood ES, Chaves I, Zheng B, Kume K, Lee CC, van der Horst GT, Hastings MH et al (2000) Interacting molecular loops in the mammalian circadian clock. Science 288:1013–1019

    CAS  PubMed  Google Scholar 

  151. Shi S, Hida A, McGuinness OP, Wasserman DH, Yamazaki S, Johnson CH (2010) Circadian clock gene Bmal1 is not essential; functional replacement with its paralog, Bmal2. Curr Biol CB 20:316–321

    CAS  PubMed  Google Scholar 

  152. Shi S, Ansari TS, McGuinness OP, Wasserman DH, Johnson CH (2013) Circadian disruption leads to insulin resistance and obesity. Curr Biol CB 23:372–381

    CAS  PubMed  Google Scholar 

  153. Shi T, Papay RS, Perez DM (2016a) α1A-Adrenergic receptor prevents cardiac ischemic damage through PKCδ/GLUT1/4-mediated glucose uptake. J Recept Signal Transduct Res 36:261–270

    PubMed  Google Scholar 

  154. Shi Y, Shu Z-J, Xue X, Yeh C-K, Katz MS, Kamat A (2016b) β2-Adrenergic receptor ablation modulates hepatic lipid accumulation and glucose tolerance in aging mice. Exp Gerontol 78:32–38

    CAS  PubMed  Google Scholar 

  155. Shigeyoshi Y, Taguchi K, Yamamoto S, Takekida S, Yan L, Tei H, Moriya T, Shibata S, Loros JJ, Dunlap JC et al (1997) Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript. Cell 91:1043–1053

    CAS  PubMed  Google Scholar 

  156. Siepka SM, Yoo S-H, Park J, Song W, Kumar V, Hu Y, Lee C, Takahashi JS (2007) Circadian mutant Overtime reveals F-box protein FBXL3 regulation of cryptochrome and period gene expression. Cell 129:1011–1023

    CAS  PubMed  PubMed Central  Google Scholar 

  157. Silver R, LeSauter J, Tresco PA, Lehman MN (1996) A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 382:810–813

    CAS  PubMed  Google Scholar 

  158. Smale L, Lee T, Nunez AA (2003) Mammalian diurnality: some facts and gaps. J Biol Rhythm 18:356–366

    Google Scholar 

  159. Sookoian S, Castaño G, Gemma C, Gianotti T-F, Pirola C-J (2007) Common genetic variations in CLOCK transcription factor are associated with nonalcoholic fatty liver disease. World J Gastroenterol: WJG 13:4242–4248

    CAS  PubMed  Google Scholar 

  160. Sookoian S, Gemma C, Gianotti TF, Burgueño A, Castaño G, Pirola CJ (2008) Genetic variants of Clock transcription factor are associated with individual susceptibility to obesity. Am J Clin Nutr 87:1606–1615

    CAS  PubMed  Google Scholar 

  161. Sun ZS, Albrecht U, Zhuchenko O, Bailey J, Eichele G, Lee CC (1997) RIGUI, a putative mammalian ortholog of the Drosophila period gene. Cell 90:1003–1011

    CAS  PubMed  Google Scholar 

  162. Sun Z, Feng D, Everett LJ, Bugge A, Lazar MA (2011) Circadian epigenomic remodeling and hepatic lipogenesis: lessons from HDAC3. Cold Spring Harb Symp Quant Biol 76:49–55

    CAS  PubMed  PubMed Central  Google Scholar 

  163. Sun Z, Miller RA, Patel RT, Chen J, Dhir R, Wang H, Zhang D, Graham MJ, Unterman TG, Shulman GI et al (2012) Hepatic Hdac3 promotes gluconeogenesis by repressing lipid synthesis and sequestration. Nat Med 18:934–942

    CAS  PubMed  PubMed Central  Google Scholar 

  164. Sun Z, Feng D, Fang B, Mullican SE, You S-H, Lim H-W, Everett LJ, Nabel CS, Li Y, Selvakumaran V et al (2013) Deacetylase-independent function of HDAC3 in transcription and metabolism requires nuclear receptor corepressor. Mol Cell 52:769–782

    CAS  PubMed  Google Scholar 

  165. Suwazono Y, Dochi M, Sakata K, Okubo Y, Oishi M, Tanaka K, Kobayashi E, Nogawa K (2008) Shift work is a risk factor for increased blood pressure in Japanese men: a 14-year historical cohort study. Hypertens Dallas Tex 1979 52:581–586

    CAS  Google Scholar 

  166. Takahashi JS (2017) Transcriptional architecture of the mammalian circadian clock. Nat Rev Genet 18:164–179

    CAS  PubMed  Google Scholar 

  167. Takeda N, Maemura K (2016) Circadian clock and the onset of cardiovascular events. Hypertens Res Off J Jpn Soc Hypertens 39:383–390

    CAS  Google Scholar 

  168. Tei H, Okamura H, Shigeyoshi Y, Fukuhara C, Ozawa R, Hirose M, Sakaki Y (1997) Circadian oscillation of a mammalian homologue of the Drosophila period gene. Nature 389:512–516

    CAS  PubMed  Google Scholar 

  169. Tognini P, Murakami M, Liu Y, Eckel-Mahan KL, Newman JC, Verdin E, Baldi P, Sassone-Corsi P (2017) Distinct circadian signatures in liver and gut clocks revealed by ketogenic diet. Cell Metab 26:523–538.e5

    CAS  PubMed  Google Scholar 

  170. Tsai J-Y, Villegas-Montoya C, Boland BB, Blasier Z, Egbejimi O, Gonzalez R, Kueht M, McElfresh TA, Brewer RA, Chandler MP et al (2013) Influence of dark phase restricted high fat feeding on myocardial adaptation in mice. J Mol Cell Cardiol 55:147–155

    CAS  PubMed  Google Scholar 

  171. Tso CF, Simon T, Greenlaw AC, Puri T, Mieda M, Herzog ED (2017) Astrocytes regulate daily rhythms in the suprachiasmatic nucleus and behavior. Curr Biol CB 27:1055–1061

    CAS  PubMed  Google Scholar 

  172. Tsuneki H, Murata S, Anzawa Y, Soeda Y, Tokai E, Wada T, Kimura I, Yanagisawa M, Sakurai T, Sasaoka T (2008) Age-related insulin resistance in hypothalamus and peripheral tissues of orexin knockout mice. Diabetologia 51:657–667

    CAS  PubMed  Google Scholar 

  173. Tsuneki H, Tokai E, Nakamura Y, Takahashi K, Fujita M, Asaoka T, Kon K, Anzawa Y, Wada T, Takasaki I et al (2015) Hypothalamic orexin prevents hepatic insulin resistance via daily bidirectional regulation of autonomic nervous system in mice. Diabetes 64:459–470

    CAS  PubMed  Google Scholar 

  174. Tsuneki H, Sasaoka T, Sakurai T (2016) Sleep control, GPCRs, and glucose metabolism. Trends Endocrinol Metab 27:633–642

    CAS  PubMed  Google Scholar 

  175. Tsuzaki K, Kotani K, Sano Y, Fujiwara S, Takahashi K, Sakane N (2010) The association of the Clock 3111 T/C SNP with lipids and lipoproteins including small dense low-density lipoprotein: results from the Mima study. BMC Med Genet 11:150

    PubMed  PubMed Central  Google Scholar 

  176. Ueta CB, Fernandes GW, Capelo LP, Fonseca TL, Maculan FD, Gouveia CHA, Brum PC, Christoffolete MA, Aoki MS, Lancellotti CL et al (2012) β(1) Adrenergic receptor is key to cold- and diet-induced thermogenesis in mice. J Endocrinol 214:359–365

    CAS  PubMed  PubMed Central  Google Scholar 

  177. Um JH, Yang S, Yamazaki S, Kang H, Viollet B, Foretz M, Chung JH (2007) Activation of 5’-AMP-activated kinase with diabetes drug metformin induces casein kinase Iepsilon (CKIepsilon)-dependent degradation of clock protein mPer2. J Biol Chem 282:20794–20798

    CAS  PubMed  Google Scholar 

  178. Van Cauter E, Désir D, Decoster C, Féry F, Balasse EO (1989) Nocturnal decrease in glucose tolerance during constant glucose infusion. J Clin Endocrinol Metab 69:604–611

    PubMed  Google Scholar 

  179. Vitaterna MH, King DP, Chang AM, Kornhauser JM, Lowrey PL, McDonald JD, Dove WF, Pinto LH, Turek FW, Takahashi JS (1994) Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior. Science 264:719–725

    CAS  PubMed  PubMed Central  Google Scholar 

  180. Vrang N, Larsen PJ, Mikkelsen JD (1995) Direct projection from the suprachiasmatic nucleus to hypophysiotrophic corticotropin-releasing factor immunoreactive cells in the paraventricular nucleus of the hypothalamus demonstrated by means of Phaseolus vulgaris-leucoagglutinin tract tracing. Brain Res 684:61–69

    CAS  PubMed  Google Scholar 

  181. Welsh DK, Takahashi JS, Kay SA (2010) Suprachiasmatic nucleus: cell autonomy and network properties. Annu Rev Physiol 72:551–577

    CAS  PubMed  PubMed Central  Google Scholar 

  182. Woon PY, Kaisaki PJ, Bragança J, Bihoreau M-T, Levy JC, Farrall M, Gauguier D (2007) Aryl hydrocarbon receptor nuclear translocator-like (BMAL1) is associated with susceptibility to hypertension and type 2 diabetes. Proc Natl Acad Sci U S A 104:14412–14417

    CAS  PubMed  PubMed Central  Google Scholar 

  183. Yasumoto Y, Hashimoto C, Nakao R, Yamazaki H, Hiroyama H, Nemoto T, Yamamoto S, Sakurai M, Oike H, Wada N et al (2016) Short-term feeding at the wrong time is sufficient to desynchronize peripheral clocks and induce obesity with hyperphagia, physical inactivity and metabolic disorders in mice. Metabolism 65:714–727

    CAS  PubMed  Google Scholar 

  184. Yi C-X, Serlie MJ, Ackermans MT, Foppen E, Buijs RM, Sauerwein HP, Fliers E, Kalsbeek A (2009) A major role for perifornical orexin neurons in the control of glucose metabolism in rats. Diabetes 58:1998–2005

    CAS  PubMed  PubMed Central  Google Scholar 

  185. Yi C-X, la Fleur SE, Fliers E, Kalsbeek A (2010) The role of the autonomic nervous liver innervation in the control of energy metabolism. Biochim Biophys Acta 1802:416–431

    CAS  PubMed  Google Scholar 

  186. Yin L, Lazar MA (2005) The orphan nuclear receptor Rev-erbalpha recruits the N-CoR/histone deacetylase 3 corepressor to regulate the circadian Bmal1 gene. Mol Endocrinol Baltim Md 19:1452–1459

    CAS  Google Scholar 

  187. Zhang W, Bi S (2015) hypothalamic regulation of brown adipose tissue thermogenesis and energy homeostasis. Front Endocrinol 6:136

    Google Scholar 

  188. Zhao X, Hirota T, Han X, Cho H, Chong L-W, Lamia K, Liu S, Atkins AR, Banayo E, Liddle C et al (2016) Circadian amplitude regulation via FBXW7-Targeted REV-ERBα degradation. Cell 165:1644–1657

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We apologize to colleagues whose work we failed to include due to an oversight on our part. The authors’ laboratories are supported by the National Institute of Health (ES027544 and CA215591) and American Heart Association (30970064).

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Ding, G., Gong, Y., Eckel-Mahan, K.L., Sun, Z. (2018). Central Circadian Clock Regulates Energy Metabolism. In: Wu, Q., Zheng, R. (eds) Neural Regulation of Metabolism. Advances in Experimental Medicine and Biology, vol 1090. Springer, Singapore. https://doi.org/10.1007/978-981-13-1286-1_5

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