Circadian Integration of Metabolism and Energetics

Circadian clocks align behavioral and biochemical processes with the day/night cycle. Nearly all vertebrate cells possess self-sustained clocks that couple endogenous rhythms with changes in cellular environment. Genetic disruption of clock genes in mice perturbs metabolic functions of specific tissues at distinct phases of the sleep/wake cycle. Circadian desynchrony, a characteristic of shift work and sleep disruption in humans, also leads to metabolic pathologies. Here, we review advances in understanding the interrelationship among circadian disruption, sleep deprivation, obesity, and diabetes and implications for rational therapeutics for these conditions.

[1]  Steven A. Brown,et al.  Resetting of circadian time in peripheral tissues by glucocorticoid signaling. , 2000, Science.

[2]  J. Gimble,et al.  Expression Profile of mRNAs Encoding Core Circadian Regulatory Proteins in Human Subcutaneous Adipose Tissue: Correlation with Age and Body Mass Index , 2009, International Journal of Obesity.

[3]  C. Saper,et al.  Hypothalamic regulation of sleep and circadian rhythms , 2005, Nature.

[4]  K. Yamamoto,et al.  Glucocorticoid regulation of the circadian clock modulates glucose homeostasis , 2009, Proceedings of the National Academy of Sciences.

[5]  Dmitri A. Nusinow,et al.  Cryptochrome Mediates Circadian Regulation of cAMP Signaling and Hepatic Gluconeogenesis , 2010, Nature Medicine.

[6]  R. Cone,et al.  The Melanocortin-3 Receptor Is Required for Entrainment to Meal Intake , 2008, The Journal of Neuroscience.

[7]  Satchidananda Panda,et al.  Network Features of the Mammalian Circadian Clock , 2009, PLoS biology.

[8]  Paolo Sassone-Corsi,et al.  The NAD+-Dependent Deacetylase SIRT1 Modulates CLOCK-Mediated Chromatin Remodeling and Circadian Control , 2008, Cell.

[9]  Jiandie D. Lin,et al.  Transcriptional coactivator PGC-1α integrates the mammalian clock and energy metabolism , 2007, Nature.

[10]  Daniel B. Forger,et al.  Emergence of Noise-Induced Oscillations in the Central Circadian Pacemaker , 2010, PLoS biology.

[11]  Satchidananda Panda,et al.  Harmonics of Circadian Gene Transcription in Mammals , 2009, PLoS genetics.

[12]  Y Sakaki,et al.  Entrainment of the circadian clock in the liver by feeding. , 2001, Science.

[13]  U. Schibler,et al.  A Serum Shock Induces Circadian Gene Expression in Mammalian Tissue Culture Cells , 1998, Cell.

[14]  Kai-Florian Storch,et al.  Physiological significance of a peripheral tissue circadian clock , 2008, Proceedings of the National Academy of Sciences.

[15]  F. Gachon,et al.  Circadian clock-coordinated 12 Hr period rhythmic activation of the IRE1alpha pathway controls lipid metabolism in mouse liver. , 2010, Cell metabolism.

[16]  J. Takahashi,et al.  cAMP-Dependent Signaling as a Core Component of the Mammalian Circadian Pacemaker , 2008, Science.

[17]  R. Eckel,et al.  Induction of Circadian Gene Expression in Human Subcutaneous Adipose‐derived Stem Cells , 2007, Obesity.

[18]  C. Fontaine,et al.  Regulation of bile acid synthesis by the nuclear receptor Rev-erbalpha. , 2008, Gastroenterology.

[19]  Andrew I. Su,et al.  A Genome-wide RNAi Screen for Modifiers of the Circadian Clock in Human Cells , 2009, Cell.

[20]  Weimin He,et al.  Nuclear Receptor Expression Links the Circadian Clock to Metabolism , 2006, Cell.

[21]  Christian Gieger,et al.  New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk , 2010, Nature Genetics.

[22]  G. Reed,et al.  Vascular Disease in Mice With a Dysfunctional Circadian Clock , 2009, Circulation.

[23]  A. Sehgal,et al.  Regulation of CLOCK and MOP4 by Nuclear Hormone Receptors in the Vasculature A Humoral Mechanism to Reset a Peripheral Clock , 2001, Cell.

[24]  A. Adamantidis,et al.  Sleep and metabolism: shared circuits, new connections , 2008, Trends in Endocrinology & Metabolism.

[25]  J. Takahashi,et al.  Circadian Clock Feedback Cycle Through NAMPT-Mediated NAD+ Biosynthesis , 2009, Science.

[26]  Kathryn Moynihan Ramsey,et al.  High-fat diet disrupts behavioral and molecular circadian rhythms in mice. , 2007, Cell metabolism.

[27]  Joseph Fogerty,et al.  Loss of Nocturnin, a circadian deadenylase, confers resistance to hepatic steatosis and diet-induced obesity , 2007, Proceedings of the National Academy of Sciences.

[28]  Tom S. Price,et al.  Circadian variation of blood pressure and the vascular response to asynchronous stress , 2007, Proceedings of the National Academy of Sciences.

[29]  Fred W. Turek,et al.  Obesity and Metabolic Syndrome in Circadian Clock Mutant Mice , 2005, Science.

[30]  Tom S. Price,et al.  Genetic Components of the Circadian Clock Regulate Thrombogenesis In Vivo , 2008, Circulation.

[31]  Ueli Schibler,et al.  System-Driven and Oscillator-Dependent Circadian Transcription in Mice with a Conditionally Active Liver Clock , 2007, PLoS biology.

[32]  B. Staels,et al.  The nuclear receptors Rev-erbs and RORs integrate circadian rhythms and metabolism , 2008, Diabetes & vascular disease research.

[33]  Ueli Schibler,et al.  The Orphan Nuclear Receptor REV-ERBα Controls Circadian Transcription within the Positive Limb of the Mammalian Circadian Oscillator , 2002, Cell.

[34]  M. Adamo,et al.  Nocturnin suppresses igf1 expression in bone by targeting the 3' untranslated region of igf1 mRNA. , 2010, Endocrinology.

[35]  Erin L. McDearmon,et al.  The genetics of mammalian circadian order and disorder: implications for physiology and disease , 2008, Nature Reviews Genetics.

[36]  Ueli Schibler,et al.  REV-ERBα Participates in Circadian SREBP Signaling and Bile Acid Homeostasis , 2009, PLoS biology.

[37]  Florian Kreppel,et al.  SIRT1 Regulates Circadian Clock Gene Expression through PER2 Deacetylation , 2008, Cell.

[38]  P. Sassone-Corsi,et al.  Circadian Control of the NAD+ Salvage Pathway by CLOCK-SIRT1 , 2009, Science.

[39]  C. Ackert-Bicknell,et al.  A circadian-regulated gene, Nocturnin, promotes adipogenesis by stimulating PPAR-γ nuclear translocation , 2010, Proceedings of the National Academy of Sciences.

[40]  A. Kalsbeek,et al.  Circadian Control of the Daily Plasma Glucose Rhythm: An Interplay of GABA and Glutamate , 2008, PloS one.

[41]  Joseph S. Takahashi,et al.  Disruption of the Clock Components CLOCK and BMAL 1 Leads to Hypoinsulinemia and Diabetes , 2012 .

[42]  T. Sakurai,et al.  Enhanced orexin receptor-2 signaling prevents diet-induced obesity and improves leptin sensitivity. , 2009, Cell metabolism.

[43]  F. Turek,et al.  Circadian Timing of Food Intake Contributes to Weight Gain , 2009, Obesity.

[44]  W. Roesler,et al.  The liver-enriched transcription factor D-site-binding protein activates the promoter of the phosphoenolpyruvate carboxykinase gene in hepatoma cells. , 1992, The Journal of biological chemistry.

[45]  Anthony Hall,et al.  Plant Circadian Clocks Increase Photosynthesis, Growth, Survival, and Competitive Advantage , 2005, Science.

[46]  T. Kondo,et al.  Reconstitution of Circadian Oscillation of Cyanobacterial KaiC Phosphorylation in Vitro , 2005, Science.

[47]  F. Turek,et al.  Sleep-wake regulation is altered in leptin-resistant (db/db) genetically obese and diabetic mice. , 2008, American journal of physiology. Regulatory, integrative and comparative physiology.

[48]  M. Young,et al.  The cardiomyocyte circadian clock: emerging roles in health and disease. , 2010, Circulation research.

[49]  F. Scheer,et al.  Adverse metabolic and cardiovascular consequences of circadian misalignment , 2009, Proceedings of the National Academy of Sciences.

[50]  S. McKnight,et al.  NPAS2: A Gas-Responsive Transcription Factor , 2002, Science.

[51]  Rachel Leproult,et al.  Slow-wave sleep and the risk of type 2 diabetes in humans , 2008, Proceedings of the National Academy of Sciences.

[52]  E. Peschke,et al.  Evidence for a circadian rhythm of insulin release from perifused rat pancreatic islets , 1998, Diabetologia.

[53]  J. Ripperger,et al.  The mammalian clock component PERIOD2 coordinates circadian output by interaction with nuclear receptors. , 2010, Genes & development.

[54]  L. Groop,et al.  Melatonin receptors in pancreatic islets: good morning to a novel type 2 diabetes gene , 2009, Diabetologia.

[55]  J. Beckmann,et al.  Circadian regulation of islet genes involved in insulin production and secretion , 2004, Molecular and Cellular Endocrinology.

[56]  M. Polansky,et al.  Disruption of circadian insulin secretion is associated with reduced glucose uptake in first-degree relatives of patients with type 2 diabetes. , 1999, Diabetes.

[57]  C. Johnson,et al.  Regulation of the PAI-1 promoter by circadian clock components: differential activation by BMAL1 and BMAL2. , 2003, Journal of molecular and cellular cardiology.

[58]  U. Schibler,et al.  Poly(ADP-Ribose) Polymerase 1 Participates in the Phase Entrainment of Circadian Clocks to Feeding , 2010, Cell.

[59]  R. Hermida,et al.  CIRCADIAN PATTERN OF AMBULATORY BLOOD PRESSURE IN UNTREATED HYPERTENSIVE PATIENTS WITH AND WITHOUT METABOLIC SYNDROME , 2009, Chronobiology international.

[60]  P. Puigserver,et al.  Fasting-dependent glucose and lipid metabolic response through hepatic sirtuin 1 , 2007, Proceedings of the National Academy of Sciences.

[61]  K. Polonsky,et al.  Abnormal patterns of insulin secretion in non-insulin-dependent diabetes mellitus. , 1988, The New England journal of medicine.

[62]  S. Panda,et al.  AMPK Regulates the Circadian Clock by Cryptochrome Phosphorylation and Degradation , 2009, Science.

[63]  M. Bucan,et al.  Nuclear Receptor Corepressor-Histone Deacetylase 3 Governs Circadian Metabolic Physiology , 2008, Nature.

[64]  Jared Rutter,et al.  Metabolism and the control of circadian rhythms. , 2002, Annual review of biochemistry.

[65]  S. Shibata,et al.  Attenuating Effect of Clock Mutation on Triglyceride Contents in the ICR Mouse Liver under a High-Fat Diet , 2007, Journal of biological rhythms.

[66]  Joseph S. Takahashi,et al.  Temperature as a Universal Resetting Cue for Mammalian Circadian Oscillators , 2010, Science.

[67]  Emmanuel Mignot,et al.  The role of hypocretins (orexins) in sleep regulation and narcolepsy. , 2002, Annual review of neuroscience.

[68]  Gregor Eichele,et al.  Adrenal glucocorticoids have a key role in circadian resynchronization in a mouse model of jet lag. , 2010, The Journal of clinical investigation.