Peripheral oscillators: the driving force for food‐anticipatory activity

Food‐anticipatory activity (FAA) and especially the food‐entrained oscillator (FEO) have driven many scientists to seek their mechanisms and locations. Starting our research on FAA we, possibly like many other scientists, were convinced that clock genes held the key to the location and the underlying mechanisms for FAA. In this review, which is aimed especially at discussing the contribution of the peripheral oscillators, we have put together the accumulating evidence that the clock gene machinery as we know it today is not sufficient to explain food entrainment. We discuss the contribution of three types of oscillating processes: (i) within the suprachiasmatic nucleus (SCN), neurons capable of maintaining a 24‐h oscillation in electrical activity driven by a set of clock genes; (ii) oscillations in metabolic genes and clock genes in other parts of the brain and in peripheral organs driven by the SCN or by food, which damp out after a few cycles; (iii) an FEO which, we propose, is a system built up of different oscillatory processes and consisting of an as‐yet‐unidentified network of central and peripheral structures. In view of the evidence that clock genes and metabolic oscillations are not essential for the persistence of FAA we propose that food entrainment is initiated by a repeated metabolic state of scarcity that drives an oscillating network of brain nuclei in interaction with peripheral oscillators. This complex may constitute the proposed FEO and is distributed in our peripheral organs as well as within the central nervous system.

[1]  Kai-Florian Storch,et al.  Daily rhythms of food-anticipatory behavioral activity do not require the known circadian clock , 2009, Proceedings of the National Academy of Sciences.

[2]  W. Engeland,et al.  Splanchnic neural activity modulates ultradian and circadian rhythms in adrenocortical secretion in awake rats. , 1994, Neuroendocrinology.

[3]  S. Shibata,et al.  Restricted feeding entrains liver clock without participation of the suprachiasmatic nucleus , 2001, Genes to cells : devoted to molecular & cellular mechanisms.

[4]  F. Stephan,et al.  Circadian Food Anticipation Persists in Capsaicin Deafferented Rats , 1998, Journal of biological rhythms.

[5]  A. Dulloo,et al.  Uncoupling proteins: their roles in adaptive thermogenesis and substrate metabolism reconsidered , 2001, British Journal of Nutrition.

[6]  S. Honma,et al.  Critical role of food amount for prefeeding corticosterone peak in rats. , 1983, The American journal of physiology.

[7]  Ralph E. Mistlberger,et al.  Circadian food-anticipatory activity: Formal models and physiological mechanisms , 1994, Neuroscience & Biobehavioral Reviews.

[8]  C. Escobar,et al.  Expectancy for food or expectancy for chocolate reveals timing systems for metabolism and reward , 2008, Neuroscience.

[9]  T. Takumi,et al.  Robust Food Anticipatory Activity in BMAL1-Deficient Mice , 2009, PloS one.

[10]  M. Caba,et al.  The rabbit pup, a natural model of nursing‐anticipatory activity , 2009, The European journal of neuroscience.

[11]  T. Tamai,et al.  Zebrafish circadian clocks: cells that see light. , 2005, Biochemical Society transactions.

[12]  M. K. Gordon,et al.  Hormonal and metabolic rhythms associated with the daily scheduled nursing in rabbit pups. , 2008, American journal of physiology. Regulatory, integrative and comparative physiology.

[13]  R. Aguilar-Roblero,et al.  Persistence of metabolic rhythmicity during fasting and its entrainment by restricted feeding schedules in rats. , 1998, American journal of physiology. Regulatory, integrative and comparative physiology.

[14]  R. Curi,et al.  Metabolic changes of twenty weeks food-restriction schedule in rats , 1986, Physiology & Behavior.

[15]  A. Kalsbeek,et al.  The suprachiasmatic nucleus controls the daily variation of plasma glucose via the autonomic output to the liver: are the clock genes involved? , 2005, The European journal of neuroscience.

[16]  A. Kalsbeek,et al.  A Suprachiasmatic Nucleus Generated Rhythm In Basal Glucose Concentrations , 1999, Journal of neuroendocrinology.

[17]  S. Yamaguchi,et al.  Control Mechanism of the Circadian Clock for Timing of Cell Division in Vivo , 2003, Science.

[18]  R. Aguilar-Roblero,et al.  Dissociation between adipose tissue signals, behavior and the food-entrained oscillator. , 2004, The Journal of endocrinology.

[19]  M. Saito,et al.  Circadian rhythms of digestive enzymes in the small intestine of the rat. II. Effects of fasting and refeeding. , 1976, Journal of biochemistry.

[20]  A. Kalsbeek,et al.  Minireview: Circadian control of metabolism by the suprachiasmatic nuclei. , 2007, Endocrinology.

[21]  C. Escobar,et al.  A daily palatable meal without food deprivation entrains the suprachiasmatic nucleus of rats , 2005, The European journal of neuroscience.

[22]  Yoko Satoh,et al.  Time-restricted feeding entrains daily rhythms of energy metabolism in mice. , 2006, American journal of physiology. Regulatory, integrative and comparative physiology.

[23]  A. Lityńska,et al.  Daily changes of protein synthesis and secretion rates in rat liver slices. , 1986, The International journal of biochemistry.

[24]  M. Menaker,et al.  Circadian Rhythms in Cultured Mammalian Retina , 1996, Science.

[25]  Toshiyuki Okano,et al.  Glucose Down-regulates Per1 and Per2mRNA Levels and Induces Circadian Gene Expression in Cultured Rat-1 Fibroblasts* 210 , 2002, The Journal of Biological Chemistry.

[26]  R. Hudson,et al.  Metabolic correlates of the circadian pattern of suckling-associated arousal in young rabbits , 2000, Journal of Comparative Physiology A.

[27]  R. Mistlberger,et al.  Neonatal monosodium glutamate alters circadian organization of feeding, food anticipatory activity and photic masking in the rat , 1999, Brain Research.

[28]  R. Aguilar-Roblero,et al.  Anticipatory changes in liver metabolism and entrainment of insulin, glucagon, and corticosterone in food-restricted rats. , 2000, American journal of physiology. Regulatory, integrative and comparative physiology.

[29]  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.

[30]  R. Buijs,et al.  Ventromedial arcuate nucleus communicates peripheral metabolic information to the suprachiasmatic nucleus. , 2006, Endocrinology.

[31]  S. Shibata,et al.  Altered food-anticipatory activity rhythm in Cryptochrome-deficient mice , 2005, Neuroscience Research.

[32]  L. Rossetti,et al.  Minireview: nutrient sensing and the regulation of insulin action and energy balance. , 2003, Endocrinology.

[33]  A. Kalsbeek,et al.  Effects of Nocturnal Light on (Clock) Gene Expression in Peripheral Organs: A Role for the Autonomic Innervation of the Liver , 2009, PloS one.

[34]  F. Stephan Calories Affect Zeitgeber Properties of the Feeding Entrained Circadian Oscillator , 1997, Physiology & Behavior.

[35]  R. Buijs,et al.  Unpredictable feeding schedules unmask a system for daily resetting of behavioural and metabolic food entrainment , 2007, The European journal of neuroscience.

[36]  R. Hernández-Muñoz,et al.  RATS MADE CIRRHOTIC BY CHRONIC CCl4 TREATMENT STILL EXHIBIT ANTICIPATORY ACTIVITY TO A RESTRICTED FEEDING SCHEDULE , 2002, Chronobiology international.

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

[38]  C. Sisk,et al.  Anticipation of 24-hr feeding schedules in rats with lesions of the suprachiasmatic nucleus. , 1979, Behavioral and neural biology.

[39]  E. Fox A genetic approach for investigating vagal sensory roles in regulation of gastrointestinal function and food intake , 2006, Autonomic Neuroscience.

[40]  Ook Joon Yoo,et al.  PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[41]  A. Dulloo,et al.  Interorgan signaling between adipose tissue metabolism and skeletal muscle uncoupling protein homologs: is there a role for circulating free fatty acids? , 1998, Diabetes.

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

[43]  Kazuyuki Shinohara,et al.  Acute Physical Stress Elevates Mouse Period1 mRNA Expression in Mouse Peripheral Tissues via a Glucocorticoid-responsive Element* , 2005, Journal of Biological Chemistry.

[44]  R. Aguilar-Roblero,et al.  Metabolic adaptations of liver mitochondria during restricted feeding schedules. , 2005, American journal of physiology. Gastrointestinal and liver physiology.

[45]  O. Shafer Blind clocks reveal elusive light input pathway in Drosophila , 2001, Trends in Neurosciences.

[46]  R C BOLLES,et al.  The rat's adjustment to a-diurnal feeding cycles. , 1962, Journal of comparative and physiological psychology.

[47]  K. Yagita,et al.  Alterations of Circadian Expressions of Clock Genes in Dahl Salt-Sensitive Rats Fed a High-Salt Diet , 2003, Hypertension.

[48]  K. Oishi,et al.  Per2 gene expressions in the suprachiasmatic nucleus and liver differentially respond to nutrition factors in rats. , 2005, JPEN. Journal of parenteral and enteral nutrition.

[49]  B. Aragona,et al.  Persistence of meal-entrained circadian rhythms following area postrema lesions in the rat , 2001, Physiology & Behavior.

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

[51]  B. Lemmer,et al.  Circadian rhythm of the in vitro stimulation of adenylate cyclase in rat heart tissue. , 1989, European journal of pharmacology.

[52]  Steven A. Brown,et al.  Rhythms of Mammalian Body Temperature Can Sustain Peripheral Circadian Clocks , 2002, Current Biology.

[53]  H. Katagiri,et al.  Neuronal pathway from the liver modulates energy expenditure and systemic insulin sensitivity , 2006, Autonomic Neuroscience.

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

[55]  C. Comperatore,et al.  Effects of vagotomy on entrainment of activity rhythms to food access , 1990, Physiology & Behavior.

[56]  S. L. la Fleur,et al.  The hepatic vagus mediates fat-induced inhibition of diabetic hyperphagia. , 2003, Diabetes.

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

[58]  S. Shibata,et al.  Adrenergic regulation of clock gene expression in mouse liver , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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

[60]  D. Krieger,et al.  Suprachiasmatic nuclear lesions do not abolish food-shifted circadian adrenal and temperature rhythmicity. , 1977, Science.

[61]  M. Dolnikoff,et al.  Metabolic consequences of food restriction in rats , 1981, Physiology & Behavior.

[62]  A. Kalsbeek,et al.  Daily rhythms in metabolic liver enzymes and plasma glucose require a balance in the autonomic output to the liver. , 2008, Endocrinology.

[63]  W. Jeffery,et al.  Conservation of retinal circadian rhythms during cavefish eye degeneration , 2006, Evolution & development.

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

[65]  R. Curi,et al.  Metabolic changes caused by irregular-feeding schedule as compared with meal-feeding , 1989, Physiology & Behavior.

[66]  F. Halberg,et al.  Circadian Rhythm in the in vitro Response of Mouse Adrenal to Adrenocorticotropic Hormone , 1962, Science.

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

[68]  M. Menaker,et al.  Is the food‐entrainable circadian oscillator in the digestive system? , 2003, Genes, brain, and behavior.

[69]  M. Harrington,et al.  Visualizing jet lag in the mouse suprachiasmatic nucleus and peripheral circadian timing system , 2009, The European journal of neuroscience.

[70]  C. Escobar,et al.  Internal desynchronization in a model of night-work by forced activity in rats , 2008, Neuroscience.

[71]  J. Brewer,et al.  Differential control of peripheral circadian rhythms by suprachiasmatic-dependent neural signals. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[72]  D. Krieger,et al.  Food and water restriction shifts corticosterone, temperature, activity and brain amine periodicity. , 1974, Endocrinology.

[73]  S. Shibata,et al.  Night-time restricted feeding normalises clock genes and Pai-1 gene expression in the db/db mouse liver , 2004, Diabetologia.

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

[75]  A. Kalsbeek,et al.  The suprachiasmatic nucleus-paraventricular nucleus interactions: a bridge to the neuroendocrine and autonomic nervous system. , 1998, Progress in brain research.

[76]  S. Reppert,et al.  Coordination of circadian timing in mammals , 2002, Nature.

[77]  E. Wagner,et al.  The Molecular Clock Mediates Leptin-Regulated Bone Formation , 2005, Cell.

[78]  F. Stephan,et al.  Plasma Glucagon, Glucose, Insulin, and Motilin in Rats Anticipating Daily Meals , 1999, Physiology & Behavior.

[79]  F. Stephan,et al.  The “Other” Circadian System: Food as a Zeitgeber , 2002, Journal of biological rhythms.

[80]  A. Kalsbeek,et al.  Restricted Daytime Feeding Modifies Suprachiasmatic Nucleus Vasopressin Release in Rats , 1998, Journal of biological rhythms.

[81]  P. Havel Peripheral Signals Conveying Metabolic Information to the Brain: Short-Term and Long-Term Regulation of Food Intake and Energy Homeostasis , 2001, Experimental biology and medicine.

[82]  R. Aguilar-Roblero,et al.  Liver 5'-deiodinase activity is modified in rats under restricted feeding schedules: evidence for post-translational regulation. , 2003, Journal of Endocrinology.

[83]  H. Romijn,et al.  Anatomical and functional demonstration of a multisynaptic suprachiasmatic nucleus adrenal (cortex) pathway , 1999, The European journal of neuroscience.

[84]  A. Kalsbeek,et al.  Hypothalamic integration of central and peripheral clocks , 2001, Nature Reviews Neuroscience.

[85]  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.