A time to fast, a time to feast: The crosstalk between metabolism and the circadian clock

The cyclic environmental conditions brought about by the 24 h rotation of the earth have allowed the evolution of endogenous circadian clocks that control the temporal alignment of behaviour and physiology, including the uptake and processing of nutrients. Both metabolic and circadian regulatory systems are built upon a complex feedback network connecting centres of the central nervous system and different peripheral tissues. Emerging evidence suggests that circadian clock function is closely linked to metabolic homeostasis and that rhythm disruption can contribute to the development of metabolic disease. At the same time, metabolic processes feed back into the circadian clock, affecting clock gene expression and timing of behaviour. In this review, we summarize the experimental evidence for this bimodal interaction, with a focus on the molecular mechanisms mediating this exchange, and outline the implications for clock-based and metabolic diseases.

[1]  R. Mistlberger.  Circadian regulation of sleep in mammals: Role of the suprachiasmatic nucleus , 2005, Brain Research Reviews.

[2]  M. Lazar,et al.  Bifunctional Role of Rev-erbα in Adipocyte Differentiation , 2008, Molecular and Cellular Biology.

[3]  Ueli Schibler,et al.  Circadian rhythms: mechanisms and therapeutic implications. , 2007, Annual review of pharmacology and toxicology.

[4]  Carl Hirschie Johnson,et al.  The Adaptive Value of Circadian Clocks An Experimental Assessment in Cyanobacteria , 2004, Current Biology.

[5]  M. Bray,et al.  Circadian rhythms in the development of obesity: potential role for the circadian clock within the adipocyte , 2007, Obesity reviews : an official journal of the International Association for the Study of Obesity.

[6]  F. Turek,et al.  Sleep and circadian rhythms: Key components in the regulation of energy metabolism , 2008, FEBS letters.

[7]  Cheng Chi Lee,et al.  Reciprocal regulation of haem biosynthesis and the circadian clock in mammals , 2004, Nature.

[8]  Ueli Schibler,et al.  Properties, Entrainment, and Physiological Functions of Mammalian Peripheral Oscillators , 2006, Journal of biological rhythms.

[9]  D. Gauguier.  Polymorphisms in aryl hydrocarbon receptor nuclear translocator-like (Arntl, Bmal1) are associated with Type 2 diabetes and hypertension , 2007 .

[10]  L. Miraglia,et al.  A Functional Genomics Strategy Reveals Rora as a Component of the Mammalian Circadian Clock , 2004, Neuron.

[11]  C. Shaw,et al.  Disruption of the circadian clock within the cardiomyocyte influences myocardial contractile function, metabolism, and gene expression. , 2008, American journal of physiology. Heart and circulatory physiology.

[12]  W. Wahli,et al.  PPARα and liver circadian clock Reciprocal regulation of BMAL1 and PPARα defines a novel positive feedback loop in the rodent liver circadian clock , 2007 .

[13]  R. Cooksey,et al.  The role of mPer2 clock gene in glucocorticoid and feeding rhythms. , 2009, Endocrinology.

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

[15]  Philippe Lefebvre,et al.  Sorting out the roles of PPARα in energy metabolism and vascular homeostasis , 2006 .

[16]  C S Pittendrigh,et al.  Temporal organization: reflections of a Darwinian clock-watcher. , 1993, Annual review of physiology.

[17]  S. Mandrup,et al.  The orphan nuclear receptor Rev-Erbalpha is a peroxisome proliferator-activated receptor (PPAR) gamma target gene and promotes PPARgamma-induced adipocyte differentiation. , 2003, The Journal of biological chemistry.

[18]  M. Bihoreau,et al.  Aryl hydrocarbon receptor nuclear translocator-like (BMAL1) is associated with susceptibility to hypertension and type 2 diabetes , 2007, Proceedings of the National Academy of Sciences.

[19]  G. Tsujimoto,et al.  Light activates the adrenal gland: timing of gene expression and glucocorticoid release. , 2005, Cell metabolism.

[20]  F. Fleury-Olela,et al.  Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. , 2000, Genes & development.

[21]  A. Carter,et al.  Association between polymorphisms in the Clock gene, obesity and the metabolic syndrome in man , 2008, International Journal of Obesity.

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

[23]  U. Schibler,et al.  Glucocorticoid hormones inhibit food‐induced phase‐shifting of peripheral circadian oscillators , 2001, The EMBO journal.

[24]  R. Foster,et al.  Circadian vision , 2007, Current Biology.

[25]  C. R. McClung,et al.  Enhanced Fitness Conferred by Naturally Occurring Variation in the Circadian Clock , 2003, Science.

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

[27]  S. Shimba,et al.  Brain and muscle Arnt-like protein-1 (BMAL1), a component of the molecular clock, regulates adipogenesis. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[28]  A J Scheen,et al.  Roles of circadian rhythmicity and sleep in human glucose regulation. , 1997, Endocrine reviews.

[29]  K. Spiegel,et al.  Impact of sleep debt on metabolic and endocrine function , 1999, The Lancet.

[30]  W. Wahli,et al.  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. , 2006, Molecular endocrinology.

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

[32]  M. Hilton,et al.  Independent circadian and sleep/wake regulation of adipokines and glucose in humans. , 2005, The Journal of clinical endocrinology and metabolism.

[33]  E. Raspé,et al.  Identification of Reverb as a physiological repressor of apoC-III gene transcription 1 , 2002 .

[34]  Anne Newman,et al.  Diabetes and sleep disturbances: findings from the Sleep Heart Health Study. , 2003, Diabetes care.

[35]  M. Suchard,et al.  Alterations in the dynamics of circulating ghrelin, adiponectin, and leptin in human obesity. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[37]  Yohei Hayashi,et al.  Rhythmic messenger ribonucleic acid expression of clock genes and adipocytokines in mouse visceral adipose tissue. , 2005, Endocrinology.

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

[39]  Jared Rutter,et al.  Regulation of Clock and NPAS2 DNA Binding by the Redox State of NAD Cofactors , 2001, Science.

[40]  Gunter Schumann,et al.  The clock gene Per2 influences the glutamatergic system and modulates alcohol consumption , 2005, Nature Medicine.

[41]  G. E. Duffield,et al.  DNA Microarray Analyses of Circadian Timing: The Genomic Basis of Biological Time , 2003, Journal of neuroendocrinology.

[42]  Joseph S. Takahashi,et al.  The Meter of Metabolism , 2008, Cell.

[43]  G. Muscat,et al.  RORalpha regulates the expression of genes involved in lipid homeostasis in skeletal muscle cells: caveolin-3 and CPT-1 are direct targets of ROR. , 2004, The Journal of biological chemistry.

[44]  A. Nakashima,et al.  Effects of fasting and re-feeding on the expression of Dec1, Per1, and other clock-related genes. , 2006, Journal of biochemistry.

[45]  Satchidananda Panda,et al.  BMAL1 and CLOCK, Two Essential Components of the Circadian Clock, Are Involved in Glucose Homeostasis , 2004, PLoS biology.

[46]  J. Gimble,et al.  Food entrainment of circadian gene expression altered in PPARalpha-/- brown fat and heart. , 2007, Biochemical and biophysical research communications.

[47]  B. Staels,et al.  Sorting out the roles of PPAR alpha in energy metabolism and vascular homeostasis. , 2006, The Journal of clinical investigation.

[48]  K. Spiegel,et al.  Brief Communication: Sleep Curtailment in Healthy Young Men Is Associated with Decreased Leptin Levels, Elevated Ghrelin Levels, and Increased Hunger and Appetite , 2004, Annals of Internal Medicine.

[49]  F. Scheer,et al.  Organization of circadian functions: interaction with the body. , 2006, Progress in brain research.

[50]  R. A. Reid,et al.  Rev-erbα, a Heme Sensor That Coordinates Metabolic and Circadian Pathways , 2007, Science.

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

[52]  S. Mandrup,et al.  The Orphan Nuclear Receptor Rev-Erbα Is a Peroxisome Proliferator-activated Receptor (PPAR) γ Target Gene and Promotes PPARγ-induced Adipocyte Differentiation* , 2003, Journal of Biological Chemistry.

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

[54]  H. Katagiri,et al.  Obesity alters circadian expressions of molecular clock genes in the brainstem , 2009, Brain Research.

[55]  S. Kay,et al.  Molecular bases of circadian rhythms. , 2001, Annual review of cell and developmental biology.

[56]  G. Eichele,et al.  The circadian rhythm of glucocorticoids is regulated by a gating mechanism residing in the adrenal cortical clock. , 2006, Cell metabolism.

[57]  V. Laudet,et al.  Fibrates increase human REV-ERBalpha expression in liver via a novel peroxisome proliferator-activated receptor response element. , 1999, Molecular endocrinology.

[58]  Christoph Handschin,et al.  Metabolic control through the PGC-1 family of transcription coactivators. , 2005, Cell metabolism.

[59]  J. Takahashi,et al.  Molecular components of the mammalian circadian clock. , 2006, Human molecular genetics.

[60]  M. Hussain,et al.  Clock is important for food and circadian regulation of macronutrient absorption in mice , 2009, Journal of Lipid Research.

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

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

[63]  M. Antoch,et al.  Early aging and age-related pathologies in mice deficient in BMAL1, the core componentof the circadian clock. , 2006, Genes & development.

[64]  M. Ikeda,et al.  CLOCK/BMAL1 is involved in lipid metabolism via transactivation of the peroxisome proliferator-activated receptor (PPAR) response element. , 2005, Journal of atherosclerosis and thrombosis.

[65]  M. Wittmann,et al.  Social Jetlag: Misalignment of Biological and Social Time , 2006, Chronobiology international.

[66]  F. Turek,et al.  Altered sleep regulation in leptin-deficient mice. , 2006, American journal of physiology. Regulatory, integrative and comparative physiology.

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