Advances in understanding the peripheral circadian clocks

In the past decade, it has become increasingly evident that the circadian clock system plays an important role in many physiological processes. The circadian clock can be divided into 2 parts: the central clock, residing in the suprachiasmatic nucleus of the hypothalamus, which receives light cues, and the peripheral clocks that reside in various tissues throughout the body. The peripheral clocks play an integral and unique role in each of their respective tissues, driving the circadian expression of specific genes involved in a variety of physiological functions. The goal of this review is to provide an introduction to and overview of the peripheral clocks, including potential mechanisms, targets, and implications for disease states. The peripheral clocks include the cardiovascular, metabolic, endocrine, immune, and reproductive systems.— Richards, J., Gumz, M. L. Advances in understanding the peripheral circadian clocks. FASEB J. 26, 3602–3613 (2012). www.fasebj.org

[1]  C. Ling,et al.  Regulation of core clock genes in human islets. , 2012, Metabolism: clinical and experimental.

[2]  S. Pradervand,et al.  The circadian clock modulates renal sodium handling. , 2012, Journal of the American Society of Nephrology.

[3]  L. Jeffers,et al.  The Circadian Protein Period 1 Contributes to Blood Pressure Control and Coordinately Regulates Renal Sodium Transport Genes , 2012, Hypertension.

[4]  C. Borchers,et al.  Adora2b-elicited Per2 stabilization promotes a HIF-dependent metabolic switch critical for myocardial adaptation to ischemia , 2012, Nature Medicine.

[5]  Pierre Baldi,et al.  Coordination of the transcriptome and metabolome by the circadian clock , 2012, Proceedings of the National Academy of Sciences.

[6]  D. Sarkar,et al.  Chronic Shift-Lag Alters the Circadian Clock of NK Cells and Promotes Lung Cancer Growth in Rats , 2012, The Journal of Immunology.

[7]  Saptarsi M. Haldar,et al.  Klf15 orchestrates circadian nitrogen homeostasis. , 2012, Cell metabolism.

[8]  M. Hughes,et al.  Circadian expression of clock genes in mouse macrophages, dendritic cells, and B cells , 2012, Brain, Behavior, and Immunity.

[9]  E. Fikrig,et al.  The circadian clock controls toll-like receptor 9-mediated innate and adaptive immunity. , 2012, Immunity.

[10]  S. Cook,et al.  Circadian variations of ischemic burden among patients with myocardial infarction undergoing primary percutaneous coronary intervention. , 2012, American heart journal.

[11]  I. Nisoli,et al.  E4BP4: an unexpected player in the immune response. , 2012, Trends in immunology.

[12]  Angel Nadal,et al.  The clock gene Rev-erbα regulates pancreatic β-cell function: modulation by leptin and high-fat diet. , 2012, Endocrinology.

[13]  Steven A. Brown,et al.  The human circadian metabolome , 2012, Proceedings of the National Academy of Sciences.

[14]  David S. Rosenbaum,et al.  Circadian rhythms govern cardiac repolarization and arrhythmogenesis , 2012, Nature.

[15]  T. Henry,et al.  Circadian Dependence of Infarct Size and Left Ventricular Function After ST Elevation Myocardial Infarction , 2012, Circulation research.

[16]  H. Kondo,et al.  Comparison of β-Adrenergic and Glucocorticoid Signaling on Clock Gene and Osteoblast-Related Gene Expressions in Human Osteoblast , 2012, Chronobiology international.

[17]  G. Curhan,et al.  Rotating night shift work and disparate hypertension risk in African–Americans , 2012, Journal of hypertension.

[18]  K. Esser,et al.  A non-canonical E-box within the MyoD core enhancer is necessary for circadian expression in skeletal muscle , 2011, Nucleic acids research.

[19]  N. Cermakian,et al.  Circadian Variation of the Response of T Cells to Antigen , 2011, The Journal of Immunology.

[20]  R. Evans,et al.  Cryptochromes mediate rhythmic repression of the glucocorticoid receptor , 2011, Nature.

[21]  M. Mizuno,et al.  Angiotensin receptor blockers shift the circadian rhythm of blood pressure by suppressing tubular sodium reabsorption. , 2011, American journal of physiology. Renal physiology.

[22]  Ke Ma,et al.  Loss of Bmal1 leads to uncoupling and impaired glucose-stimulated insulin secretion in β-cells , 2011, Islets.

[23]  Gene D. Block,et al.  Disruption of Circadian Rhythms Accelerates Development of Diabetes through Pancreatic Beta-Cell Loss and Dysfunction , 2011, Journal of biological rhythms.

[24]  Sooyoung Chung,et al.  The adrenal peripheral clock: Glucocorticoid and the circadian timing system , 2011, Frontiers in Neuroendocrinology.

[25]  D. Weaver,et al.  The period of the circadian oscillator is primarily determined by the balance between casein kinase 1 and protein phosphatase 1 , 2011, Proceedings of the National Academy of Sciences.

[26]  Xia Wang,et al.  MiR-206-mediated dynamic mechanism of the mammalian circadian clock , 2011, BMC Systems Biology.

[27]  K. Bottum,et al.  Aryl Hydrocarbon Receptor Deficiency Enhances Insulin Sensitivity and Reduces PPAR-α Pathway Activity in Mice , 2011, Environmental health perspectives.

[28]  A. Fontana,et al.  A timetable of 24-hour patterns for human lymphocyte subpopulations. , 2011, Journal of biological regulators and homeostatic agents.

[29]  Sooyoung Chung,et al.  Circadian rhythm of adrenal glucocorticoid: its regulation and clinical implications. , 2011, Biochimica et biophysica acta.

[30]  Koji Maemura,et al.  Circadian clock and cardiovascular disease. , 2011, Journal of cardiology.

[31]  Xiaoling Li,et al.  Sirtuin 1 in lipid metabolism and obesity , 2011, Annals of medicine.

[32]  P. Konturek,et al.  Gut clock: implication of circadian rhythms in the gastrointestinal tract. , 2011, Journal of physiology and pharmacology : an official journal of the Polish Physiological Society.

[33]  Michelle L. Gumz,et al.  The circadian clock in the kidney. , 2011, Journal of the American Society of Nephrology : JASN.

[34]  I. Pernicova,et al.  An endocrinologist's guide to the clock. , 2011, The Journal of clinical endocrinology and metabolism.

[35]  C. Green,et al.  Post-transcriptional control of circadian rhythms , 2011, Journal of Cell Science.

[36]  K. Yamamoto,et al.  Circadian Rhythm Gene Period 3 Is an Inhibitor of the Adipocyte Cell Fate* , 2011, The Journal of Biological Chemistry.

[37]  L. Ghibelli,et al.  Melatonin: a pleiotropic molecule regulating inflammation. , 2010, Biochemical pharmacology.

[38]  Joseph S. Takahashi,et al.  Circadian Integration of Metabolism and Energetics , 2010, Science.

[39]  T. Gressley,et al.  The effect of dexamethasone on clock gene mRNA levels in bovine neutrophils and lymphocytes. , 2010, Veterinary immunology and immunopathology.

[40]  Steve A. Kay,et al.  Clocks not winding down: unravelling circadian networks , 2010, Nature Reviews Molecular Cell Biology.

[41]  M. Menaker,et al.  Circadian clocks in the ovary , 2010, Trends in Endocrinology & Metabolism.

[42]  Ueli Schibler,et al.  Cardiac hypertrophy, low blood pressure, and low aldosterone levels in mice devoid of the three circadian PAR bZip transcription factors DBP, HLF, and TEF. , 2010, American journal of physiology. Regulatory, integrative and comparative physiology.

[43]  E. Peschke,et al.  New evidence for a role of melatonin in glucose regulation. , 2010, Best practice & research. Clinical endocrinology & metabolism.

[44]  R. Hermida,et al.  INFLUENCE OF CIRCADIAN TIME OF HYPERTENSION TREATMENT ON CARDIOVASCULAR RISK: RESULTS OF THE MAPEC STUDY , 2010, Chronobiology international.

[45]  L. Stow,et al.  Regulation of αENaC expression by the circadian clock protein Period 1 in mpkCCD(c14) cells. , 2010, Biochimica et biophysica acta.

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

[47]  S. Imai.  "Clocks" in the NAD World: NAD as a metabolic oscillator for the regulation of metabolism and aging. , 2010, Biochimica et biophysica acta.

[48]  J. Takahashi,et al.  Disruption of the Clock Components CLOCK and BMAL1 Leads to Hypoinsulinemia and Diabetes , 2010, Nature.

[49]  B. Jung-Hynes,et al.  Melatonin resynchronizes dysregulated circadian rhythm circuitry in human prostate cancer cells , 2010, Journal of pineal research.

[50]  G. E. Pickard,et al.  Chronic treatment with a selective inhibitor of casein kinase I δ/ε yields cumulative phase delays in circadian rhythms , 2010, Psychopharmacology.

[51]  G. FitzGerald,et al.  Circadian Clocks and Vascular Function , 2010, Circulation research.

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

[53]  Xiaohong Song,et al.  Regulation of circadian gene expression in the kidney by light and food cues in rats. , 2010, American journal of physiology. Regulatory, integrative and comparative physiology.

[54]  U. Schibler,et al.  The mammalian circadian timing system: organization and coordination of central and peripheral clocks. , 2010, Annual review of physiology.

[55]  Robert P Light,et al.  The effect of measuring ambulatory blood pressure on nighttime sleep and daytime activity--implications for dipping. , 2010, Clinical journal of the American Society of Nephrology : CJASN.

[56]  R. Agarwal.  Regulation of circadian blood pressure: from mice to astronauts , 2010, Current opinion in nephrology and hypertension.

[57]  J. Dyck,et al.  Short Communication: Ischemia/Reperfusion Tolerance Is Time-of-Day–Dependent: Mediation by the Cardiomyocyte Circadian Clock , 2009, Circulation research.

[58]  S. Pradervand,et al.  Molecular clock is involved in predictive circadian adjustment of renal function , 2009, Proceedings of the National Academy of Sciences.

[59]  D. Pfaff,et al.  Stomach ghrelin-secreting cells as food-entrainable circadian clocks , 2009, Proceedings of the National Academy of Sciences.

[60]  D. Weaver,et al.  The circadian clock protein Period 1 regulates expression of the renal epithelial sodium channel in mice. , 2009, The Journal of clinical investigation.

[61]  G. Ko,et al.  Circadian regulation of ion channels and their functions , 2009, Journal of neurochemistry.

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

[63]  L. Muglia,et al.  Impaired steroidogenesis and implantation failure in Bmal1-/- mice. , 2009, Endocrinology.

[64]  Ryusuke Okura,et al.  Circadian expression of the Na+/H+ exchanger NHE3 in the mouse renal medulla. , 2009, Biomedical research.

[65]  F. Gonzalez,et al.  Vascular PPARgamma controls circadian variation in blood pressure and heart rate through Bmal1. , 2008, Cell metabolism.

[66]  T. Todo,et al.  Role of angiotensin and the clock system in the circadian regulation of plasminogen activator inhibitor-1. , 2008, The Kobe journal of medical sciences.

[67]  A. Sehgal,et al.  The Circadian Clock Protein BMAL1 Is Necessary for Fertility and Proper Testosterone Production in Mice , 2008, Journal of biological rhythms.

[68]  E. Challet,et al.  Minireview: Entrainment of the suprachiasmatic clockwork in diurnal and nocturnal mammals. , 2007, Endocrinology.

[69]  K. Oishi,et al.  Thrombomodulin Is a Clock-controlled Gene in Vascular Endothelial Cells* , 2007, Journal of Biological Chemistry.

[70]  Kathryn S Lilley,et al.  Glucocorticoid signaling synchronizes the liver circadian transcriptome , 2007, Hepatology.

[71]  K. Nagai,et al.  Autonomic and cardiovascular responses to scent stimulation are altered in cry KO mice , 2007, Neuroscience Letters.

[72]  Molly S Bray,et al.  The Circadian Clock within the Cardiomyocyte Is Essential for Responsiveness of the Heart to Fatty Acids* , 2006, Journal of Biological Chemistry.

[73]  J. Hannibal,et al.  Diurnal rhythmicity of the clock genes Per1 and Per2 in the rat ovary. , 2006, Endocrinology.

[74]  A. Tamakoshi,et al.  A prospective cohort study of shift work and risk of ischemic heart disease in Japanese male workers. , 2006, American journal of epidemiology.

[75]  Eric L Bittman,et al.  Suprachiasmatic Regulation of Circadian Rhythms of Gene Expression in Hamster Peripheral Organs: Effects of Transplanting the Pacemaker , 2006, The Journal of Neuroscience.

[76]  R. Palme,et al.  Impaired daily glucocorticoid rhythm in Per1Brd mice , 2006, Journal of Comparative Physiology A.

[77]  D. Franchimont.  Overview of the Actions of Glucocorticoids on the Immune Response: A Good Model to Characterize New Pathways of Immunosuppression for New Treatment Strategies , 2004, Annals of the New York Academy of Sciences.

[78]  D. Diogo,et al.  Influence of Two Doses of Irbesartan on Non‐Dipper Circadian Blood Pressure Rhythm in Salt‐Sensitive Black Hypertensives Under High Salt Diet , 2003, Journal of cardiovascular pharmacology.

[79]  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.

[80]  N. Despotović.  Blood pressure circadian rhythm and obesity: Blood pressure variations and obesity , 2002 .

[81]  Kai-Florian Storch,et al.  Extensive and divergent circadian gene expression in liver and heart , 2002, Nature.

[82]  A. Kalsbeek,et al.  Role for the Pineal and Melatonin in Glucose Homeostasis: Pinealectomy Increases Night‐Time Glucose Concentrations , 2001, Journal of neuroendocrinology.

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

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

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

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

[87]  P. Larochelle.  Circadian Variation in Blood Pressure: Dipper or Nondipper , 2000, Journal of clinical hypertension.

[88]  E. Eide,et al.  Nuclear Entry of the Circadian Regulator mPER1 Is Controlled by Mammalian Casein Kinase I ɛ , 2000, Molecular and Cellular Biology.

[89]  T H Monk,et al.  What Can the Chronobiologist Do to Help the Shift Worker? , 2000, Journal of biological rhythms.

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

[91]  D. P. King,et al.  Role of the CLOCK protein in the mammalian circadian mechanism. , 1998, Science.

[92]  Yoshiyuki Sakaki,et al.  Circadian oscillation of a mammalian homologue of the Drosophila period gene , 1997, Nature.

[93]  T. Uzu,et al.  Diuretics shift circadian rhythm of blood pressure from nondipper to dipper in essential hypertension. , 1997, Circulation.

[94]  V. Gribkoff,et al.  Molecular Dissection of Two Distinct Actions of Melatonin on the Suprachiasmatic Circadian Clock , 1997, Neuron.

[95]  L. Aiello,et al.  Angiotensin II induces plasminogen activator inhibitor-1 and -2 expression in vascular endothelial and smooth muscle cells. , 1995, The Journal of clinical investigation.

[96]  Julio A. Panza,et al.  Circadian variation in vascular tone and its relation to α-sympathetic vasoconstrictor activity , 1991 .

[97]  J. Redman,et al.  Free-running activity rhythms in the rat: entrainment by melatonin. , 1983, Science.

[98]  C. Dollery,et al.  Circadian rhythm of baroreflex reactivity and adrenergic vascular response. , 1980, Cardiovascular research.

[99]  R J Konopka,et al.  Clock mutants of Drosophila melanogaster. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[100]  M. Kaneko,et al.  Circadian variation in human peripheral blood flow levels and exercise responses. , 1968, Journal of applied physiology.

[101]  I. Johnston,et al.  Circadian expression of clock and putative clock-controlled genes in skeletal muscle of the zebrafish. , 2012, American journal of physiology. Regulatory, integrative and comparative physiology.

[102]  A. Lerchl,et al.  Temporal Control of Spermatogenesis Is Independent of the Central Circadian Pacemaker in Djungarian Hamsters (Phodopus sungorus)1 , 2011, Biology of reproduction.

[103]  A. Bukowska.  [Anticarcinogenic role of melatonin--potential mechanisms]. , 2011, Medycyna pracy.

[104]  G. Tsujimoto,et al.  Salt-sensitive hypertension in circadian clock–deficient Cry-null mice involves dysregulated adrenal Hsd3b6 , 2010, Nature Medicine.

[105]  Daniel B. Forger,et al.  Reversible protein phosphorylation regulates circadian rhythms. , 2007, Cold Spring Harbor symposia on quantitative biology.

[106]  U. Albrecht.  The mammalian circadian clock: a network of gene expression. , 2004, Frontiers in bioscience : a journal and virtual library.

[107]  P. Sassone-Corsi,et al.  No circadian rhythms in testis: Period1 expression is clock independent and developmentally regulated in the mouse. , 2003, Molecular endocrinology.

[108]  N. Despotović.  [Circadian rhythm of blood pressure and obesity--blood pressure variation and obesity]. , 2002, Medicinski pregled.

[109]  A. Quyyumi,et al.  Circadian variation in vascular tone and its relation to alpha-sympathetic vasoconstrictor activity. , 1991, The New England journal of medicine.