Journal of Genetics

, Volume 87, Issue 5, pp 447–458 | Cite as

Energy-responsive timekeeping

  • David A. Bechtold
Review Article


An essential component of energy homeostasis lies in an organism’s ability to coordinate daily patterns in activity, feeding, energy utilization and energy storage across the daily 24-h cycle. Most tissues of the body contain the molecular clock machinery required for circadian oscillation and rhythmic gene expression. Under normal circumstances, behavioural and physiological rhythms are orchestrated and synchronized by the suprachiasmatic nucleus (SCN) of the hypothalamus, considered to be the master circadian clock. However, metabolic processes are easily decoupled from the primarily light-driven SCN when food intake is desynchronized from normal diurnal patterns of activity. This dissociation from SCN based timing demonstrates that the circadian system is responsive to changes in energy supply and metabolic status. There has long been evidence for the existence of an anatomically distinct and autonomous food-entrainable oscillator (FEO) that can govern behavioural rhythms, when feeding becomes the dominant entraining stimulus. But now rapidly growing evidence suggests that core circadian clock genes are involved in reciprocal transcriptional feedback with genetic regulators of metabolism, and are directly responsive to cellular energy supply. This close interaction is likely to be critical for normal circadian regulation of metabolism, and may also underlie the disruption of proper metabolic rhythms observed in metabolic disorders, such as obesity and type-II diabetes.


circadian rhythm FEO food anticipation metabolism PGC-1α PPAR SIRT1 metabolic syndrome type-II diabetes 


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  1. Abe M., Herzog E. D., Yamazaki S., Straume M., Tei H., Sakaki Y. et al. 2002 Circadian rhythms in isolated brain regions. J. Neurosci. 22, 350–356.PubMedGoogle Scholar
  2. Adelmant G., Begue A., Stehelin D. and Laudet V. 1996 A functional Rev-erb alpha responsive element located in the human Rev-erb alpha promoter mediates a repressing activity. Proc. Natl. Acad. Sci. USA 93, 3553–3558.PubMedCrossRefGoogle Scholar
  3. Akhtar R. A., Reddy A. B., Maywood E. S., Clayton J. D., King V. M., Smith A. G. et al. 2002 Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr. Biol. 12, 540–550.PubMedCrossRefGoogle Scholar
  4. Ando H., Yanagihara H., Hayashi Y., Obi Y., Tsuruoka S., Takamura T. et al. 2005 Rhythmic messenger ribonucleic acid expression of clock genes and adipocytokines in mouse visceral adipose tissue. Endocrinology 146, 5631–5636.PubMedCrossRefGoogle Scholar
  5. Angeles-Castellanos M., Aguilar-Roblero R. and Escobar C. 2004 c-Fos expression in hypothalamic nuclei of food-entrained rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 286, R158–R165.PubMedGoogle Scholar
  6. Asher G., Gatfield D., Stratmann M., Reinke H., Dibner C., Kreppel F. et al. 2008 SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134, 317–328.PubMedCrossRefGoogle Scholar
  7. Balsalobre A., Brown S. A., Marcacci L., Tronche F., Kellendonk C., Reichardt H. M. et al. 2000 Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289, 2344–2347.PubMedCrossRefGoogle Scholar
  8. Bando H., Nishio T., van der Horst G. T., Masubuchi S., Hisa Y. and Okamura H. 2007 Vagal regulation of respiratory clocks in mice. J. Neurosci. 27, 4359–4365.PubMedCrossRefGoogle Scholar
  9. Bartness T. J., Song C. K. and Demas G. E. 2001 SCN efferents to peripheral tissues: implications for biological rhythms. J. Biol. Rhythms 16, 196–204.PubMedCrossRefGoogle Scholar
  10. Baur J. A., Pearson K. J., Price N. L., Jamieson H. A., Lerin C., Kalra A. et al. 2006 Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444, 337–342.PubMedCrossRefGoogle Scholar
  11. Bechtold D. A., Brown T. M., Luckman S. M. and Piggins H. D. 2008 Metabolic rhythm abnormalities in mice lacking VIPVPAC2 signaling. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R344–R351.PubMedGoogle Scholar
  12. Berthoud H. R. 2002 Multiple neural systems controlling food intake and body weight. Neurosci. Biobehav. Rev. 26, 393–428.PubMedCrossRefGoogle Scholar
  13. Blundell J. E. and Gillett A. 2001 Control of food intake in the obese. Obes. Res. 9,suppl. 4, 263S–270S.PubMedCrossRefGoogle Scholar
  14. Boden G., Chen X. and Polansky M. 1999 Disruption of circadian insulin secretion is associated with reduced glucose uptake in first-degree relatives of patients with type 2 diabetes. Diabetes 48, 2182–2188.PubMedCrossRefGoogle Scholar
  15. Bordone L., Motta M. C., Picard F., Robinson A., Jhala U. S., Apfeld J. et al. 2006 Sirt1 regulates insulin secretion by repressing UCP2 in pancreatic beta cells. PLoS Biol. 4, e31.PubMedCrossRefGoogle Scholar
  16. Boulos Z. and Terman M. 1980 Food availability and daily biological rhythms. Neurosci. Biobehav. Rev. 4, 119–131.PubMedCrossRefGoogle Scholar
  17. Brunet A., Sweeney L. B., Sturgill J. F., Chua K. F., Greer P. L., Lin Y. et al. 2004 Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303, 2011–2015.PubMedCrossRefGoogle Scholar
  18. Buijs R. M. and Kreier F. 2006 The metabolic syndrome: a brain disease? J. Neuroendocrinol. 18, 715–716.PubMedCrossRefGoogle Scholar
  19. Cailotto C., van Heijningen C., van der Vliet J., van der Plasse G., Habold C., Kalsbeek A. et al. 2008 Daily rhythms in metabolic liver enzymes and plasma glucose require a balance in the autonomic output to the liver. Endocrinology 149, 1914–1925.PubMedCrossRefGoogle Scholar
  20. Calvani M., Scarfone A., Granato L., Mora E. V., Nanni G., Castagneto M. et al. 2004 Restoration of adiponectin pulsatility in severely obese subjects after weight loss. Diabetes 53, 939–947.PubMedCrossRefGoogle Scholar
  21. Canaple L., Rambaud J., Dkhissi-Benyahya O., Rayet B., Tan N. S., Michalik L. et al. 2006 Reciprocal regulation of brain and muscle Arnt-like protein 1 and peroxisome proliferator-activated receptor alpha defines a novel positive feedback loop in the rodent liver circadian clock. Mol. Endocrinol. 20, 1715–1727.PubMedCrossRefGoogle Scholar
  22. Carling D. 2007 The role of the AMP-activated protein kinase in the regulation of energy homeostasis. Novartis Found. Symp. 286, 72–81; discussion 81–85.PubMedCrossRefGoogle Scholar
  23. Cermakian N. and Sassone-Corsi P. 2002 Environmental stimulus perception and control of circadian clocks. Curr. Opin. Neurobiol. 12, 359–365.PubMedCrossRefGoogle Scholar
  24. Chaput J. P., Brunet M. and Tremblay A. 2006 Relationship between short sleeping hours and childhood overweight/obesity: results from the ‘Quebec en Forme’ Project. Int. J. Obes. (London) 30, 1080–1085.CrossRefGoogle Scholar
  25. Chawla A. and Lazar M. A. 1993 Induction of Rev-ErbA alpha, an orphan receptor encoded on the opposite strand of the alphathyroid hormone receptor gene, during adipocyte differentiation. J. Biol. Chem. 268, 16265–16269.PubMedGoogle Scholar
  26. Chen M. P., Chung F. M., Chang D. M., Tsai J. C., Huang H. F., Shin S. J. and Lee Y. J. 2006 Elevated plasma level of visfatin/pre-B cell colony-enhancing factor in patients with type 2 diabetes mellitus. J. Clin. Endocrinol. Metab. 91, 295–299.PubMedCrossRefGoogle Scholar
  27. Comperatore C. A. and Stephan F. K. 1990 Effects of vagotomy on entrainment of activity rhythms to food access. Physiol. Behav. 47, 671–678.PubMedCrossRefGoogle Scholar
  28. Cone R. D., Cowley M. A., Butler A. A., Fan W., Marks D. L. and Low M. J. 2001 The arcuate nucleus as a conduit for diverse signals relevant to energy homeostasis. Int. J. Obes. Relat. Metab. Disord. 25,suppl. 5, S63–S67.PubMedCrossRefGoogle Scholar
  29. Curtis A. M., Seo S. B., Westgate E. J., Rudic R. D., Smyth E. M., Chakravarti D. et al. 2004 Histone acetyltransferase-dependent chromatin remodeling and the vascular clock. J. Biol. Chem. 279, 7091–7097.PubMedCrossRefGoogle Scholar
  30. Dali-Youcef N., Lagouge M., Froelich S., Koehl C., Schoonjans K. and Auwerx J. 2007 Sirtuins: the ‘magnificent seven’, function, metabolism and longevity. Ann. Med. 39, 335–345.PubMedCrossRefGoogle Scholar
  31. Damiola F., Le Minh N., Preitner N., Kornmann B., Fleury-Olela F. and Schibler U. 2000 Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 14, 2950–2961.PubMedCrossRefGoogle Scholar
  32. Dasgupta B. and Milbrandt J. 2007 Resveratrol stimulates AMP kinase activity in neurons. Proc. Natl. Acad. Sci. USA 104, 7217–7222.PubMedCrossRefGoogle Scholar
  33. Davidson A. J. and Stephan F. K. 1998 Circadian food anticipation persists in capsaicin deafferented rats. J. Biol. Rhythms 13, 422–429.PubMedCrossRefGoogle Scholar
  34. Davidson A. J., Cappendijk S. L. and Stephan F. K. 2000 Feedingentrained circadian rhythms are attenuated by lesions of the parabrachial region in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278, R1296–R1304.PubMedGoogle Scholar
  35. Davidson A. J., Aragona B. J., Houpt T. A. and Stephan F. K. 2001a Persistence of meal-entrained circadian rhythms following area postrema lesions in the rat. Physiol. Behav. 74, 349–354.PubMedCrossRefGoogle Scholar
  36. Davidson A. J., Aragona B. J., Werner R. M., Schroeder E., Smith J. C. and Stephan F. K. 2001b Food-anticipatory activity persists after olfactory bulb ablation in the rat. Physiol. Behav. 72, 231–235.PubMedCrossRefGoogle Scholar
  37. Davidson A. J., Poole A. S., Yamazaki S. and Menaker M. 2003 Is the food-entrainable circadian oscillator in the digestive system? Genes Brain Behav. 2, 32–39.PubMedCrossRefGoogle Scholar
  38. Desvergne B. and Wahli W. 1999 Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr. Rev. 20, 649–688.PubMedCrossRefGoogle Scholar
  39. Doi M., Hirayama J. and Sassone-Corsi P. 2006 Circadian regulator CLOCK is a histone acetyltransferase. Cell 125, 497–508.PubMedCrossRefGoogle Scholar
  40. Dudley C. A., Erbel-Sieler C., Estill S. J., Reick M., Franken P., Pitts S. and McKnight S. L. 2003 Altered patterns of sleep and behavioral adaptability in NPAS2-deficient mice. Science 301, 379–383.PubMedCrossRefGoogle Scholar
  41. Duffield G. E., Best J. D., Meurers B. H., Bittner A., Loros J. J. and Dunlap J. C. 2002 Circadian programs of transcriptional activation, signaling, and protein turnover revealed by microarray analysis of mammalian cells. Curr. Biol. 12, 551–557.PubMedCrossRefGoogle Scholar
  42. Duez H. and Staels B. 2008 The nuclear receptors Rev-erbs and RORs integrate circadian rhythms and metabolism. Diab. Vasc. Dis. Res. 5, 82–88.PubMedCrossRefGoogle Scholar
  43. Dupré S. M., Burt D. W., Talbot R., Downing A., Mouzaki D., Waddington D. et al. 2008 Identification of melatonin-regulated genes in the ovine pituitary pars tuberalis, a target site for seasonal hormone control. Endocrinol. 149, 5527–5539.CrossRefGoogle Scholar
  44. Emery P. and Reppert S. M. 2004 A rhythmic Ror. Neuron 43, 443–446.PubMedCrossRefGoogle Scholar
  45. Etchegaray J. P., Lee C., Wade P. A. and Reppert S. M. 2003 Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature 421, 177–182.PubMedCrossRefGoogle Scholar
  46. Feillet C. A., Ripperger J. A., Magnone M. C., Dulloo A., Albrecht U. and Challet E. 2006 Lack of food anticipation in Per2 mutant mice. Curr. Biol. 16, 2016–2022.PubMedCrossRefGoogle Scholar
  47. Fontaine C., Dubois G., Duguay Y., Helledie T., Vu-Dac N., Gervois P. et al. 2003 The orphan nuclear receptor Rev-Erbalpha is a peroxisome proliferator-activated receptor (PPAR) gamma target gene and promotes PPARgamma-induced adipocyte differentiation. J. Biol. Chem. 278, 37672–37680.PubMedCrossRefGoogle Scholar
  48. Fulco M., Cen Y., Zhao P., Hoffman E. P., McBurney M. W., Sauve A. A. and Sartorelli V. 2008 Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev. Cell 14, 661–673.PubMedCrossRefGoogle Scholar
  49. Fuller P.M., Lu J. and Saper C. B. 2008 Differential rescue of lightand food-entrainable circadian rhythms. Science 320, 1074–1077.PubMedCrossRefGoogle Scholar
  50. Gallego M. and Virshup D. M. 2007 Post-translational modifications regulate the ticking of the circadian clock. Nat. Rev. Mol. Cell Biol. 8, 139–148.PubMedCrossRefGoogle Scholar
  51. Gallou-Kabani C., Vige A. and Junien C. 2007 Lifelong circadian and epigenetic drifts in metabolic syndrome. Epigenetics 2, 137–146.PubMedGoogle Scholar
  52. Gangwisch J. E., Malaspina D., Boden-Albala B. and Heymsfield S. B. 2005 Inadequate sleep as a risk factor for obesity: analyses of the NHANES I. Sleep 28, 1289–1296.PubMedGoogle Scholar
  53. Gervois P., Chopin-Delannoy S., Fadel A., Dubois G., Kosykh V., Fruchart J. C. et al. 1999 Fibrates increase human REV-ERBalpha expression in liver via a novel peroxisome proliferator-activated receptor response element. Mol. Endocrinol. 13, 400–409.PubMedCrossRefGoogle Scholar
  54. Gooley J. J., Schomer A. and Saper C. B. 2006 The dorsomedial hypothalamic nucleus is critical for the expression of food-entrainable circadian rhythms. Nat. Neurosci. 9, 398–407.PubMedCrossRefGoogle Scholar
  55. Granados-Fuentes D., Prolo L. M., Abraham U. and Herzog E. D. 2004 The suprachiasmatic nucleus entrains, but does not sustain, circadian rhythmicity in the olfactory bulb. J. Neurosci. 24, 615–619.PubMedCrossRefGoogle Scholar
  56. Guo H., Brewer J. M., Lehman M. N. and Bittman E. L. 2006 Suprachiasmatic regulation of circadian rhythms of gene expression in hamster peripheral organs: effects of transplanting the pacemaker. J. Neurosci. 26, 6406–6412.PubMedCrossRefGoogle Scholar
  57. Hirayama J., Sahar S., Grimaldi B., Tamaru T., Takamatsu K., Nakahata Y. and Sassone-Corsi P. 2007 CLOCK-mediated acetylation of BMAL1 controls circadian function. Nature 450, 1086–1090.PubMedCrossRefGoogle Scholar
  58. Hirota T., Okano T., Kokame K., Shirotani-Ikejima H., Miyata T. and 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, 44244–44251.PubMedCrossRefGoogle Scholar
  59. Iijima M., Yamaguchi S., van der Horst G. T., Bonnefont X., Okamura H. and Shibata S. 2005 Altered food-anticipatory activity rhythm in Cryptochrome-deficient mice. Neurosci. Res. 52, 166–173.PubMedCrossRefGoogle Scholar
  60. Inoue I., Shinoda Y., Ikeda M., Hayashi K., Kanazawa K., Nomura M. et al. 2005 CLOCK/BMAL1 is involved in lipid metabolism via transactivation of the peroxisome proliferator-activated receptor (PPAR) response element. J. Atheroscler. Thromb. 12, 169–174.PubMedGoogle Scholar
  61. Ishida A., Mutoh T., Ueyama T., Bando H., Masubuchi S., Nakahara D. et al. 2005 Light activates the adrenal gland: timing of gene expression and glucocorticoid release. Cell Metab. 2, 297–307.PubMedCrossRefGoogle Scholar
  62. Kaasik K. and Lee C. C. 2004 Reciprocal regulation of haem biosynthesis and the circadian clock in mammals. Nature 430, 467–471.PubMedCrossRefGoogle Scholar
  63. Kahn B. B., Alquier T., Carling D. and Hardie D. G. 2005 AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 1, 15–25.PubMedCrossRefGoogle Scholar
  64. Kalsbeek A., Kreier F., Fliers E., Sauerwein H. P., Romijn J. A. and Buijs R. M. 2007 Minireview: Circadian control of metabolism by the suprachiasmatic nuclei. Endocrinol. 148, 5635–5639.CrossRefGoogle Scholar
  65. Karlsson B., Knutsson A. and 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.PubMedCrossRefGoogle Scholar
  66. Kersten S., Seydoux J., Peters J. M., Gonzalez F. J., Desvergne B. and Wahli W. 1999 Peroxisome proliferator-activated receptor alpha mediates the adaptive response to fasting. J. Clin. Invest. 103, 1489–1498.PubMedCrossRefGoogle Scholar
  67. Kohsaka A. and Bass J. 2007 A sense of time: how molecular clocks organize metabolism. Trends Endocrinol. Metab. 18, 4–11.PubMedCrossRefGoogle Scholar
  68. Kornmann B., Schaad O., Bujard H., Takahashi J. S. and Schibler U. 2007 System-driven and oscillator-dependent circadian transcription in mice with a conditionally active liver clock. PLoS Biol. 5, e34.PubMedCrossRefGoogle Scholar
  69. Krieger D. T. 1972 Circadian corticosteroid periodicity: critical period for abolition by neonatal injection of corticosteroid. Science 178, 1205–1207.PubMedCrossRefGoogle Scholar
  70. Kudo T., Kawashima M., Tamagawa T. and Shibata S. 2008 Clock mutation facilitates accumulation of cholesterol in the liver of mice fed a cholesterol and/or cholic acid diet. Am. J. Physiol. Endocrinol. Metab. 294, E120–E130.PubMedCrossRefGoogle Scholar
  71. Laitinen S., Fontaine C., Fruchart J. C. and Staels B. 2005 The role of the orphan nuclear receptor Rev-Erb alpha in adipocyte differentiation and function. Biochimie 87, 21–25.PubMedCrossRefGoogle Scholar
  72. Lamia K. A., Storch K. F. and Weitz C. J. 2008 Physiological significance of a peripheral tissue circadian clock. Proc. Natl. Acad. Sci. USA 105, 15172–15177.PubMedCrossRefGoogle Scholar
  73. Lamont E. W., Robinson B., Stewart J. and Amir S. 2005 The central and basolateral nuclei of the amygdala exhibit opposite diurnal rhythms of expression of the clock protein Period2. Proc. Natl. Acad. Sci. USA 102, 4180–4184.PubMedCrossRefGoogle Scholar
  74. Landry G. J. and Mistlberger R. E. 2007 Food entrainment: methodological issues. J. Biol. Rhythms 22, 484–487.PubMedCrossRefGoogle Scholar
  75. Landry G. J., Simon M. M., Webb I. C. and Mistlberger R. E. 2006 Persistence of a behavioral food-anticipatory circadian rhythm following dorsomedial hypothalamic ablation in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R1527–R1534.PubMedGoogle Scholar
  76. Landry G. J., Yamakawa G. R., Webb I. C., Mear R. J. and Mistlberger R. E. 2007 The dorsomedial hypothalamic nucleus is not necessary for the expression of circadian food-anticipatory activity in rats. J. Biol. Rhythms 22, 467–478.PubMedCrossRefGoogle Scholar
  77. Laposky A. D., Bass J., Kohsaka A. and Turek F.W. 2008 Sleep and circadian rhythms: key components in the regulation of energy metabolism. FEBS Lett. 582, 142–151.PubMedCrossRefGoogle Scholar
  78. Le Minh N., Damiola F., Tronche F., Schutz G. and Schibler U. 2001 Glucocorticoid hormones inhibit food-induced phase-shifting of peripheral circadian oscillators. EMBO J. 20, 7128–7136.PubMedCrossRefGoogle Scholar
  79. Lemberger T., Saladin R., Vazquez M., Assimacopoulos F., Staels B., Desvergne B. et al. 1996 Expression of the peroxisome proliferator-activated receptor alpha gene is stimulated by stress and follows a diurnal rhythm. J. Biol. Chem. 271, 1764–1769.PubMedCrossRefGoogle Scholar
  80. Leone T. C., Lehman J. J., Finck B. N., Schaeffer P. J., Wende A. R., Boudina S. et al. 2005 PGC-1alpha deficiency causes multisystem energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 3, e101.PubMedCrossRefGoogle Scholar
  81. Li X., Zhang S., Blander G., Tse J. G., Krieger M. and Guarente L. 2007 SIRT1 deacetylates and positively regulates the nuclear receptor LXR. Mol. Cell 28, 91–106.PubMedCrossRefGoogle Scholar
  82. Liang H. and Ward W. F. 2006 PGC-1alpha: a key regulator of energy metabolism. Adv. Physiol. Educ. 30, 145–151.PubMedCrossRefGoogle Scholar
  83. Lin J., Handschin C. and Spiegelman B. M. 2005a Metabolic control through the PGC-1 family of transcription coactivators. Cell. Metab. 1, 361–370.PubMedCrossRefGoogle Scholar
  84. Lin J., Yang R., Tarr P. T., Wu P. H., Handschin C., Li S. et al. 2005b Hyperlipidemic effects of dietary saturated fats mediated through PGC-1beta coactivation of SREBP. Cell 120, 261–273.PubMedCrossRefGoogle Scholar
  85. Liu C., Li S., Liu T., Borjigin J. and Lin J. D. 2007 Transcriptional coactivator PGC-1alpha integrates the mammalian clock and energy metabolism. Nature 447, 477–481.PubMedCrossRefGoogle Scholar
  86. Loudon A. S., Meng Q. J., Maywood E. S., Bechtold D. A., Boot-Handford R. P. and Hastings M. H. 2007 The biology of the circadian Ck1epsilon tau mutation in mice and Syrian hamsters: a tale of two species. Cold. Spr. Harb. Symp. Quant. Biol. 72, 261–271.CrossRefGoogle Scholar
  87. Lowrey P. L. and Takahashi J. S. 2004 Mammalian circadian biology: elucidating genome-wide levels of temporal organization. Annu. Rev. Genomics Hum. Genet. 5, 407–441.PubMedCrossRefGoogle Scholar
  88. McCarthy J. J., Andrews J. L., McDearmon E. L., Campbell K. S., Barber B. K., Miller B. H. et al. 2007 Identification of the circadian transcriptome in adult mouse skeletal muscle. Physiol. Genomics 31, 86–95.PubMedCrossRefGoogle Scholar
  89. McNamara P., Seo S. P., Rudic R. D., Sehgal A., Chakravarti D. and FitzGerald G. A. 2001 Regulation of CLOCK and MOP4 by nuclear hormone receptors in the vasculature: a humoral mechanism to reset a peripheral clock. Cell 105, 877–889.PubMedCrossRefGoogle Scholar
  90. Meng Q. J., Logunova L., Maywood E. S., Gallego M., Lebiecki J., Brown T. M. et al. 2008 Setting clock speed in mammals: the CK1 epsilon tau mutation in mice accelerates circadian pacemakers by selectively destabilizing PERIOD proteins. Neuron 58, 78–88.PubMedCrossRefGoogle Scholar
  91. Meyer-Bernstein E. L., Jetton A. E., Matsumoto S. I., Markuns J. F., Lehman M. N. and Bittman E. L. 1999 Effects of suprachiasmatic transplants on circadian rhythms of neuroendocrine function in golden hamsters. Endocrinology 140, 207–218.PubMedCrossRefGoogle Scholar
  92. Michan S. and Sinclair D. 2007 Sirtuins in mammals: insights into their biological function. Biochem. J. 404, 1–13.PubMedCrossRefGoogle Scholar
  93. Mieda M., Williams S. C., Richardson J. A., Tanaka K. and Yanagisawa M. 2006 The dorsomedial hypothalamic nucleus as a putative food-entrainable circadian pacemaker. Proc. Natl. Acad. Sci. USA 103, 12150–12155.PubMedCrossRefGoogle Scholar
  94. Miller B. H., McDearmon E. L., Panda S., Hayes K. R., Zhang J., Andrews J. L. et al. 2007 Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. Proc. Natl. Acad. Sci. USA 104, 3342–3347.PubMedCrossRefGoogle Scholar
  95. Mistlberger R. E. 1994 Circadian food-anticipatory activity: formal models and physiological mechanisms. Neurosci. Biobehav. Rev. 18, 171–195.PubMedCrossRefGoogle Scholar
  96. Mistlberger R. E. and Marchant E. G. 1995 Computational and entrainment models of circadian food-anticipatory activity: evidence from non-24-hr feeding schedules. Behav. Neurosci. 109, 790–798.PubMedCrossRefGoogle Scholar
  97. Mistlberger R. E. and Mumby D. G. 1992 The limbic system and food-anticipatory circadian rhythms in the rat: ablation and dopamine blocking studies. Behav. Brain. Res. 47, 159–168.PubMedCrossRefGoogle Scholar
  98. Mistlberger R. E. and Rechtschaffen A. 1984 Recovery of anticipatory activity to restricted feeding in rats with ventromedial hypothalamic lesions. Physiol. Behav. 33, 227–235.PubMedCrossRefGoogle Scholar
  99. Mistlberger R. E. and Rusak B. 1988 Food-anticipatory circadian rhythms in rats with paraventricular and lateral hypothalamic ablations. J. Biol. Rhythms. 3, 277–291.CrossRefGoogle Scholar
  100. Motta M. C., Divecha N., Lemieux M., Kamel C., Chen D., Gu W. et al. 2004 Mammalian SIRT1 represses forkhead transcription factors. Cell 116, 551–563.PubMedCrossRefGoogle Scholar
  101. Nakahata Y., Grimaldi B., Sahar S., Hirayama J. and Sassone-Corsi P. 2007 Signaling to the circadian clock: plasticity by chromatin remodeling. Curr. Opin. Cell Biol. 19, 230–237.PubMedCrossRefGoogle Scholar
  102. Nakahata Y., Kaluzova M., Grimaldi B., Sahar S., Hirayama J., Chen D. et al. 2008 The NAD+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell 134, 329–340.PubMedCrossRefGoogle Scholar
  103. Naruse Y., Oh-hashi K., Iijima N., Naruse M., Yoshioka H. and Tanaka M. 2004 Circadian and light-induced transcription of clock gene Per1 depends on histone acetylation and deacetylation. Mol. Cell Biol. 24, 6278–6287.PubMedCrossRefGoogle Scholar
  104. Oishi K., Miyazaki K., Kadota K., Kikuno R., Nagase T., Atsumi G. et al. 2003 Genome-wide expression analysis of mouse liver reveals CLOCK-regulated circadian output genes. J. Biol. Chem. 278, 41519–41527.PubMedCrossRefGoogle Scholar
  105. Oishi K., Amagai N., Shirai H., Kadota K., Ohkura N. and Ishida N. 2005a Genome-wide expression analysis reveals 100 adrenal gland-dependent circadian genes in the mouse liver. DNA Res. 12, 191–202.PubMedCrossRefGoogle Scholar
  106. Oishi K., Shirai H. and Ishida N. 2005b CLOCK is involved in the circadian transactivation of peroxisome-proliferator-activated receptor alpha (PPARalpha) in mice. Biochem. J. 386, 575–581.PubMedCrossRefGoogle Scholar
  107. Oishi K., Atsumi G., Sugiyama S., Kodomari I., Kasamatsu M., Machida K. and Ishida N. 2006 Disrupted fat absorption attenuates obesity induced by a high-fat diet in Clock mutant mice. FEBS Lett. 580, 127–130.PubMedCrossRefGoogle Scholar
  108. Panda S., Antoch M. P., Miller B. H., Su A. I., Schook A. B., Straume M. et al. 2002 Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109, 307–320.PubMedCrossRefGoogle Scholar
  109. Pitts S., Perone E. and Silver R. 2003 Food-entrained circadian rhythms are sustained in arrhythmic Clk/Clk mutant mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R57–R67.PubMedGoogle Scholar
  110. Preitner N., Damiola F., Lopez-Molina L., Zakany J., Duboule D., Albrecht U. and Schibler U. 2002 The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110, 251–260.PubMedCrossRefGoogle Scholar
  111. Ralph M. R., Foster R. G., Davis F. C. and Menaker M. 1990 Transplanted suprachiasmatic nucleus determines circadian period. Science 247, 975–978.PubMedCrossRefGoogle Scholar
  112. Ramsey K. M., Marcheva B., Kohsaka A. and Bass J. 2007 The clockwork of metabolism. Annu. Rev. Nutr. 27, 219–240.PubMedCrossRefGoogle Scholar
  113. Raspe E., Duez H., Gervois P., Fievet C., Fruchart J. C., Besnard S. et al. 2001 Transcriptional regulation of apolipoprotein CIII gene expression by the orphan nuclear receptor RORalpha. J. Biol. Chem. 276, 2865–2871.PubMedCrossRefGoogle Scholar
  114. Raspe E., Duez H., Mansen A., Fontaine C., Fievet C., Fruchart J. C. et al. 2002a Identification of Rev-erbalpha as a physiological repressor of apoC-III gene transcription. J. Lipid Res. 43, 2172–2179.PubMedCrossRefGoogle Scholar
  115. Raspe E., Mautino G., Duval C., Fontaine C., Duez H., Barbier O. et al. 2002b Transcriptional regulation of human Rev-erbalpha gene expression by the orphan nuclear receptor retinoic acid-related orphan receptor alpha. J. Biol. Chem. 277, 49275–49281.PubMedCrossRefGoogle Scholar
  116. Reick M., Garcia J. A., Dudley C. and McKnight S. L. 2001 NPAS2: an analog of clock operative in the mammalian forebrain. Science 293, 506–509.PubMedCrossRefGoogle Scholar
  117. Reppert S. M. and Weaver D. R. 2002 Coordination of circadian timing in mammals. Nature 418, 935–941.PubMedCrossRefGoogle Scholar
  118. Retnakaran R., Youn B. S., Liu Y., Hanley A. J., Lee N. S., Park J. W. et al. 2008 Correlation of circulating full-length visfatin (PBEF/Nampt) with metabolic parameters in subjects with and without diabetes: a cross-sectional study. Clin. Endocrinol. (Oxf.) (in press).Google Scholar
  119. Revollo J. R., Grimm A. A. and Imai S. 2004 The NAD biosynthesis pathway mediated by nicotinamide phosphoribosyltransferase regulates Sir2 activity in mammalian cells. J. Biol. Chem. 279, 50754–50763.PubMedCrossRefGoogle Scholar
  120. Revollo J. R., Korner A., Mills K. F., Satoh A., Wang T., Garten A. et al. 2007 Nampt/PBEF/Visfatin regulates insulin secretion in beta cells as a systemic NAD biosynthetic enzyme. Cell Metab. 6, 363–375.PubMedCrossRefGoogle Scholar
  121. Ripperger J. A. and Schibler U. 2001 Circadian regulation of gene expression in animals. Curr. Opin. Cell. Biol. 13, 357–362.PubMedCrossRefGoogle Scholar
  122. Ripperger J. A. and Schibler U. 2006 Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nat. Genet. 38, 369–374.PubMedCrossRefGoogle Scholar
  123. Rodgers R. J., Ishii Y., Halford J. C. and Blundell J. E. 2002 Orexins and appetite regulation. Neuropeptides 36, 303–325.PubMedCrossRefGoogle Scholar
  124. Rodgers J. T., Lerin C., Haas W., Gygi S. P., Spiegelman B. M. and Puigserver P. 2005 Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434, 113–118.PubMedCrossRefGoogle Scholar
  125. Rodgers J. T., Lerin C., Gerhart-Hines Z. and Puigserver P. 2008 Metabolic adaptations through the PGC-1 alpha and SIRT1 pathways. FEBS Lett. 582, 46–53.PubMedCrossRefGoogle Scholar
  126. Ruiter M., Buijs R. M. and Kalsbeek A. 2006 Hormones and the autonomic nervous system are involved in suprachiasmatic nucleus modulation of glucose homeostasis. Curr. Diabetes Rev. 2, 213–226.PubMedCrossRefGoogle Scholar
  127. Rutter J., Reick M., Wu L. C. and McKnight S. L. 2001 Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science 293, 510–514.PubMedCrossRefGoogle Scholar
  128. Rutter J., Reick M. and McKnight S. L. 2002 Metabolism and the control of circadian rhythms. Annu. Rev. Biochem. 71, 307–331.PubMedCrossRefGoogle Scholar
  129. Saper C. B., Cano G. and Scammell T. E. 2005a Homeostatic, circadian, and emotional regulation of sleep. J. Comp. Neurol. 493, 92–98.PubMedCrossRefGoogle Scholar
  130. Saper C. B., Lu J., Chou T. C. and Gooley J. 2005b The hypothalamic integrator for circadian rhythms. Trends Neurosci. 28, 152–157.PubMedCrossRefGoogle Scholar
  131. Sauve A. A., Wolberger C., Schramm V. L. and Boeke J. D. 2006 The biochemistry of sirtuins. Annu. Rev. Biochem. 75, 435–465.PubMedCrossRefGoogle Scholar
  132. Sawaki Y., Nihonmatsu I. and Kawamura H. 1984 Transplantation of the neonatal suprachiasmatic nuclei into rats with complete bilateral suprachiasmatic lesions. Neurosci. Res. 1, 67–72.PubMedCrossRefGoogle Scholar
  133. Schibler U. 2003 Circadian rhythms. Liver regeneration clocks on. Science 302, 234–235.PubMedCrossRefGoogle Scholar
  134. Schibler U., Ripperger J. and Brown S. A. 2003 Peripheral circadian oscillators in mammals: time and food. J. Biol. Rhythms 18, 250–260.PubMedCrossRefGoogle Scholar
  135. Shearman L. P., Sriram S., Weaver D. R., Maywood E. S., Chaves I., Zheng B. et al. 2000 Interacting molecular loops in the mammalian circadian clock. Science 288, 1013–1019.PubMedCrossRefGoogle Scholar
  136. Silver R., LeSauter J., Tresco P. A. and Lehman M. N. 1996 A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 382, 810–813.PubMedCrossRefGoogle Scholar
  137. Stephan F. K. 2002 The “other” circadian system: food as a Zeitgeber. J. Biol. Rhythms 17, 284–292.PubMedCrossRefGoogle Scholar
  138. Stephan F. K. and Zucker I. 1972 Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc. Natl. Acad. Sci. USA 69, 1583–1586.PubMedCrossRefGoogle Scholar
  139. Stokkan K. A., Yamazaki S., Tei H., Sakaki Y. and Menaker M. 2001 Entrainment of the circadian clock in the liver by feeding. Science 291, 490–493.PubMedCrossRefGoogle Scholar
  140. Storch K. F., Lipan O., Leykin I., Viswanathan N., Davis F. C., Wong W. H. and Weitz C. J. 2002 Extensive and divergent circadian gene expression in liver and heart. Nature 417, 78–83.PubMedCrossRefGoogle Scholar
  141. Sujino M., Masumoto K. H., Yamaguchi S., van der Horst G. T., Okamura H. and Inouye S. T. 2003 Suprachiasmatic nucleus grafts restore circadian behavioral rhythms of genetically arrhythmic mice. Curr. Biol. 13, 664–668.PubMedCrossRefGoogle Scholar
  142. Teboul M., Guillaumond F., Gréchez-Cassiau A. and Delaunay F. 2008 The Nuclear hormone receptors family round the clock. Mol. Endocrinol. (in press).Google Scholar
  143. Tu B. P. and McKnight S. L. 2006 Metabolic cycles as an underlying basis of biological oscillations. Nat. Rev. Mol. Cell Biol. 7, 696–701.PubMedCrossRefGoogle Scholar
  144. Turek F. W., Joshu C., Kohsaka A., Lin E., Ivanova G., McDearmon E. et al. 2005 Obesity and metabolic syndrome in circadian Clock mutant mice. Science 308, 1043–1045.PubMedCrossRefGoogle Scholar
  145. Um J. H., Yang S., Yamazaki S., Kang H., Viollet B., Foretz M. and Chung J. H. 2007 Activation of 5′-AMP-activated kinase with diabetes drug metformin induces casein kinase I epsilon(CKIepsilon)-dependent degradation of clock protein mPer2. J. Biol. Chem. 282, 20794–20798.PubMedCrossRefGoogle Scholar
  146. Vujovic N., Davidson A. J. and Menaker M. 2008 Sympathetic input modulates, but does not determine, phase of peripheral circadian oscillators. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R355–R360.PubMedGoogle Scholar
  147. Wakamatsu H., Yoshinobu Y., Aida R., Moriya T., Akiyama M. and Shibata S. 2001 Restricted-feeding-induced anticipatory activity rhythm is associated with a phase-shift of the expression of mPer1 and mPer2 mRNA in the cerebral cortex and hippocampus but not in the suprachiasmatic nucleus of mice. Eur. J. Neurosci. 13, 1190–1196.PubMedCrossRefGoogle Scholar
  148. Walker J. R. and Hogenesch J. B. 2005 RNA profiling in circadian biology. Methods Enzymol. 393, 366–376.PubMedCrossRefGoogle Scholar
  149. Wang J. and Lazar M. A. 2008 Bifunctional role of Rev-erbalpha in adipocyte differentiation. Mol. Cell Biol. 28, 2213–2220.PubMedCrossRefGoogle Scholar
  150. Wang T., Zhang X., Bheda P., Revollo J. R., Imai S. and Wolberger C. 2006 Structure of Nampt/PBEF/visfatin, a mammalian NAD+ biosynthetic enzyme. Nat. Struct. Mol. Biol. 13, 661–662.PubMedCrossRefGoogle Scholar
  151. Wijnen H. and Young M. W. 2006 Interplay of circadian clocks and metabolic rhythms. Annu. Rev. Genet. 40, 409–448.PubMedCrossRefGoogle Scholar
  152. Wolk R. and Somers V. K. 2007 Sleep and the metabolic syndrome. Exp. Physiol. 92, 67–78.PubMedCrossRefGoogle Scholar
  153. Yang X., Lamia K. A. and Evans R. M. 2007 Nuclear receptors, metabolism, and the circadian clock. Cold. Spr. Harb. Symp. Quant. Biol. 72, 387–394.CrossRefGoogle Scholar
  154. Yang H., Yang T., Baur J. A., Perez E., Matsui T., Carmona J. J. et al. 2007 Nutrient-sensitive mitochondrial NAD+ levels dictate cell survival. Cell 130, 1095–1107.PubMedCrossRefGoogle Scholar
  155. Yildiz B. O., Suchard M. A., Wong M. L., McCann S. M. and Licinio J. 2004 Alterations in the dynamics of circulating ghrelin, adiponectin, and leptin in human obesity. Proc. Natl. Acad. Sci. USA 101, 10434–10439.PubMedCrossRefGoogle Scholar
  156. Yoo S. H., Yamazaki S., Lowrey P. L., Shimomura K., Ko C. H., Buhr E. D. et al. 2004 PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc. Natl. Acad. Sci. USA 101, 5339–5346.PubMedCrossRefGoogle Scholar
  157. Yoon J. C., Puigserver P., Chen G., Donovan J., Wu Z., Rhee J. et al. 2001 Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature 413, 131–138.PubMedCrossRefGoogle Scholar
  158. Young M. E. and Bray M. S. 2007 Potential role for peripheral circadian clock dyssynchrony in the pathogenesis of cardiovascular dysfunction. Sleep Med. 8, 656–667.PubMedCrossRefGoogle Scholar
  159. Zvonic S., Floyd Z. E., Mynatt R. L. and Gimble J. M. 2007 Circadian rhythms and the regulation of metabolic tissue function and energy homeostasis. Obesity (Silver Spr.) 15, 539–543.CrossRefGoogle Scholar

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© Indian Academy of Sciences 2008

Authors and Affiliations

  1. 1.Faculty of Life SciencesUniversity of ManchesterManchesterUK

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