Circadian clock control of endocrine factors

Nature Reviews Endocrinology

Volumn 10, Issue 8, 2014, Pages 466-475

  Gamble, Karen L ^a   Berry, Ryan ^b   Frank, Stuart J ^b   Young, Martin E ^c  

^a Division of Behavioural Neurobiology Department of Psychiatry   (United States)

^b Division of Endocrinology   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; BIOLOGICAL FACTOR; CYANOCOBALAMIN; ENDOCRINE FACTOR; GROWTH HORMONE; HYDROCORTISONE; INTRINSIC FACTOR; MELATONIN; UNCLASSIFIED DRUG;

CHRONOBIOLOGY; CIRCADIAN RHYTHM; ENDOCRINE DISEASE; ENVIRONMENTAL FACTOR; HEREDITY; HUMAN; HYPOTHALAMUS HYPOPHYSIS SYSTEM; METABOLIC SYNDROME X; NEOPLASM; NONHUMAN; OSCILLATION; PATHOLOGY; PRIORITY JOURNAL; REVIEW; SLEEP WAKING CYCLE; STIMULUS RESPONSE; SUPRACHIASMATIC NUCLEUS; TARGET ORGAN;

ADIPONECTIN; ADULT; ANIMALS; CHILD; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; ENDOCRINE SYSTEM; FEMALE; HOMEOSTASIS; HORMONES; HUMAN GROWTH HORMONE; HUMANS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MELATONIN; METABOLIC SYNDROME X; PITUITARY-ADRENAL SYSTEM; SLEEP;

EID: 84904747470     PISSN: 17595029     EISSN: 17595037     Source Type: Journal    
DOI: 10.1038/nrendo.2014.78     Document Type: Review

References (157)

1. Avram, A. M., Jaffe, C. A., Symons, K. V. & Barkan, A. L. Endogenous circulating ghrelin does not mediate growth hormone rhythmicity or response to fasting. J. Clin. Endocrinol. Metab. 90, 2982-2987 (2005).
2. Russell, W. et al. Free triiodothyronine has a distinct circadian rhythm that is delayed but parallels thyrotropin levels. J. Clin. Endocrinol. Metab. 93, 2300-2306 (2008).
3. Carroll, T., Raff, H. & Findling, J. W. Late-night salivary cortisol measurement in the diagnosis of Cushing's syndrome. Nat. Clin. Pract. Endocrinol. Metab. 4, 344-350 (2008).
4. Freeman, M. E., Kanyicska, B., Lerant, A. & Nagy, G. Prolactin: structure, function, and regulation of secretion. Physiol. Rev. 80, 1523-1631 ( 2000).
5. Walton, M. J. et al. A diurnal variation in testicular hormone production is maintained following gonadotrophin suppression in normal men. Clin. Endocrinol. 66, 123-129 (2007).
6. Goel, N. et al. Circadian rhythm profiles in women with night eating syndrome. J. Biol. Rhythms 24, 85-94 (2009).
7. Scheer, F. A. et al. Day/night variations of high-molecular-weight adiponectin and lipocalin-2 in healthy men studied under fed and fasted conditions. Diabetologia 53, 2401-2405 (2010).
8. Borjigin, J., Zhang, L. S. & Calinescu, A. A. Circadian regulation of pineal gland rhythmicity. Mol. Cell. Endocrinol. 349, 13-19 (2012).
9. Dardente, H. Melatonin-dependent timing of seasonal reproduction by the pars tuberalis: pivotal roles for long daylengths and thyroid hormones. J. Neuroendocrinol. 24, 249-266 (2012).
10. Rondanelli, M., Faliva, M. A., Perna, S. & Antoniello, N. Update on the role of melatonin in the prevention of cancer tumorigenesis and in the management of cancer correlates, such as sleep-wake and mood disturbances: review and remarks. Aging Clin. Exp. Res. 25, 499-510 (2013).
11. Slominski, R. M., Reiter, R. J., Schlabritz-Loutsevitch, N., Ostrom, R. S. & Slominski, A. T. Melatonin membrane receptors in peripheral tissues: distribution and functions. Mol. Cell. Endocrinol. 351, 152-166 (2012).
12. Bouatia-Naji, N. et al. A variant near MTNR1b is associated with increased fasting plasma glucose levels and type 2 diabetes risk. Nat. Genet. 41, 89-94 (2009).
13. Sanchez-Barcelo, E. J., Mediavilla, M. D. & Reiter, R. J. Clinical uses of melatonin in pediatrics. Int. J. Pediatr. 2011, 892624 (2011).
14. Lewy, A. J., Lefler, B. J., Emens, J. S. & Bauer, V. K. The circadian basis of winter depression. Proc. Natl Acad. Sci. USA 103, 7414-7419 (2006).
15. Dickmeis, T. Glucocorticoids and the circadian clock. J. Endocrinol. 200, 3-22 (2009).
16. Kalsbeek A, van Heerikhuize, J. J., Wortel, J. & Buijs, R. M. A diurnal rhythm of stimulatory input to the hypothalamo-pituitary-adrenal system as revealed by timed intrahypothalamic administration of the vasopressin V1 antagonist. J. Neurosci. 16, 5555-5565 (1996).
17. Gardi, J., Obal, F. Jr, Fang, J., Zhang, J. & Krueger, J. M. Diurnal variations and sleep deprivation-induced changes in rat hypothalamic GHRH and somatostatin contents. Am. J. Physiol. 277, R1339-R1344 (1999).
18. Dimaraki, E. V., Jaffe, C. A., Bowers, C. Y., Marbach, P. & Barkan, A. L. Pulsatile and nocturnal growth hormone secretions in men do not require periodic declines of somatostatin. Am. J. Physiol. Endocrinol. Metab. 285, E163-E170 (2003).
19. Takahashi, Y. Essential roles of growth hormone (GH) and insulin-like growth factor-I (IGF-I) in the liver. Endocr. J. 59, 955-962 (2012).
20. Jaffe, C. A. et al. Regulatory mechanisms of growth hormone secretion are sexually dimorphic. J. Clin. Invest. 102, 153-164 (1998).
21. Villadolid, M. C. et al. Twenty-four hour plasma, GH, FSH and LH profiles in patients with Turner's syndrome. Endocrinol. Jpn 35, 71-81 (1988).
22. Goji, K. Pulsatile characteristics of spontaneous growth hormone (GH) concentration profiles in boys evaluated by an ultrasensitive immunoradiometric assay: evidence for ultradian periodicity of GH secretion. J. Clin. Endocrinol. Metab. 76, 667-670 (1993).
23. Gavrila, A. et al. Diurnal and ultradian dynamics of serum adiponectin in healthy men: comparison with leptin, circulating soluble leptin receptor, and cortisol patterns. J. Clin. Endocrinol. Metab. 88, 2838-2843 (2003).
24. Maeda, N., Funahashi, T. & Shimomura, I. Cardiovascular-metabolic impact of adiponectin and aquaporin. Endocr. J. 60, 251-259 (2013).
25. Begg, D. P. & Woods, S. C. Interactions between the central nervous system and pancreatic islet secretions: a historical perspective. Adv. Physiol. Educ. 37, 53-60 (2013).
26. Saltiel, A. R. & Kahn, C. R. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414, 799-806 (2001).
27. Bolli, G. B. et al. Demonstration of a dawn phenomenon in normal human volunteers. Diabetes 33, 1150-1153 (1984).
28. Bolli, G. B. & Gerich, J. E. The "dawn phenomenon"-A common occurrence in both non-insulin-dependent and insulin-dependent diabetes mellitus. N. Engl. J. Med. 310, 746-750 (1984).
29. Schmidt, M. I., Lin, Q. X., Gwynne, J. T. & Jacobs, S. Fasting early morning rise in peripheral insulin: evidence of the dawn phenomenon in nondiabetes. Diabetes Care 7, 32-35 (1984).
30. Campbell, P. J., Bolli, G. B., Cryer, P. E. & Gerich, J. E. Pathogenesis of the dawn phenomenon in patients with insulin-dependent diabetes mellitus. Accelerated glucose production and impaired glucose utilization due to nocturnal surges in growth hormone secretion. N. Engl. J. Med. 312, 1473-1479 (1985).
31. Monnier, L., Colette, C., Dejager, S. & Owens, D. Magnitude of the dawn phenomenon and its impact on the overall glucose exposure in type 2 diabetes: is this of concern? Diabetes Care 36, 4057-4062 (2013).
32. Campbell, P. J., Bolli, G. B., Cryer, P. E. & Gerich, J. E. Sequence of events during development of the dawn phenomenon in insulin-dependent diabetes mellitus. Metabolism 34, 1100-1104 (1985).
33. Clark, L. A. et al. A quantitative analysis of the effects of activity and time of day on the diurnal variations of blood pressure. J. Chronic Dis. 40, 671-681 (1987).
34. Linsell, C. R., Lightman, S. L., Mullen, P. E., Brown, M. J. & Causon, R. C. Circadian rhythms of epinephrine and norepinephrine in man. J. Clin. Endocrinol. Metab. 60, 1210-1215 (1985).
35. Krauchi, K. & Wirz-Justice, A. Circadian rhythm of heat production, heart rate, and skin and core temperature under unmasking conditions in men. Am. J. Physiol. 267, R819-R829 (1994).
36. Van Cauter, E. & Spiegel, K. in Neurobiology of Sleep and Circadian Rhythms Vol. 133 (eds Turek, F. W. & Zee, P. C) 397-426 (Marcel Dekker, 1999).
37. Van Cauter, E. & Copinschi, G. in Human Growth Hormone Secretion: Basic and Clinical Research Ch. 16 (eds Smith, R. G. & Thorner, M. O) 261-283 (Humana Press, 1999).
38. Van Cauter, E. et al. Modulation of glucose regulation and insulin secretion by circadian rhythmicity and sleep. J. Clin. Invest. 88, 934-942 (1991).
39. Scheer, F. A. et al. Impact of the human circadian system, exercise, and their interaction on cardiovascular function. Proc. Natl Acad. Sci. USA 107, 20541-20546 (2010).
40. Scheer, F. A. et al. The human endogenous circadian system causes greatest platelet activation during the biological morning independent of behaviors. PLoS ONE 6, e24549 (2011).
41. Shea, S. A., Hilton, M. F., Hu, K. & Scheer, F. A. Existence of an endogenous circadian blood pressure rhythm in humans that peaks in the evening. Circ. Res. 108, 980-984 (2011).
42. Scheer, F. A. & Shea, S. A. Human circadian system causes morning peak in pro-thrombotic plasminogen activator inhibitor-1 (PAI-1) independent of sleep/wake cycle. Blood 123, 590-593 (2014).
43. Takahashi, J. S., Hong, H. K., Ko, C. H. & McDearmon, E. L. The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat. Rev. Genet. 9, 764-775 (2008).
44. Edery, I. Circadian rhythms in a nutshell. Physiol. Genomics 3, 59-74 (2000).
45. Gekakis, N. et al. Role of the clock protein in the mammalian circadian mechanism. Science 280, 1564-1569 (1998).
46. Hogenesch, J., Gu, Y., Jain, S. & Bradfield, C. The basic-helix-loop-helix-PAS orphan MOP3 forms transcriptionally active complexes with circadian and hypoxia factors. Proc. Natl Acad. Sci. USA 95, 5474-5479 (1998).
47. Zylka, M., Shearman, L., Weaver, D. & Reppert, S. Three period homologs in mammals: differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron 20, 1103-1110 (1998).
48. Miyamoto, Y. & Sancar, A. Vitamin B2-based blue-light photoreceptors in the retinohypothalamic tract as the photoactive pigments for setting the circadian clock in mammals. Proc. Natl Acad. Sci. USA 95, 6097-6102 (1998).
49. Preitner, N. et al. The orphan nuclear receptor REV-ERBα controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110, 251-260 (2002).
50. Storch, K. F. et al. Extensive and divergent circadian gene expression in liver and heart. Nature 417, 78-83 (2002).
51. McCarthy, J. J. et al. Identification of the circadian transcriptome in adult mouse skeletal muscle. Physiol. Genomics 31, 86-95 (2007).
52. Martino, T. et al. Day/night rhythms in gene expression of the normal murine heart. J. Mol. Med. 82, 256-264 (2004).
53. Cardone, L. et al. Circadian clock control by SUMOylation of BMAL1. Science 309, 1390-1394 (2005).
54. Hardin, P. E. & Yu, W. Circadian transcription: passing the hat to clock. Cell 125, 424-426 (2006).
55. Kloss, B. et al. The Drosophila clock gene doubletime encodes a protein closely related to human casein kinase Iepsilon. Cell 94, 97-107 (1998).
56. Millar, A. J. Clock proteins: turned over after hours? Curr. Biol. 10, R529-R531 (2000).
57. Asher, G. & Schibler, U. Crosstalk between components of circadian and metabolic cycles in mammals. Cell Metab. 13, 125-137 (2011).
58. Durgan, D. J. et al. O-GlcNAcylation, novel post-translational modification linking myocardial metabolism and cardiomyocyte circadian clock. J. Biol. Chem. 286, 44606-44619 (2011).
59. O'Neill, J. S. et al. Circadian rhythms persist without transcription in a eukaryote. Nature 469, 554-558 (2011).
60. Meyer-Bernstein, E. L. et al. Effects of suprachiasmatic transplants on circadian rhythms of neuroendocrine function in golden hamsters. Endocrinology 140, 207-218 (1999).
61. Coomans, C. P. et al. The suprachiasmatic nucleus controls circadian energy metabolism and hepatic insulin sensitivity. Diabetes 62, 1102-1108 (2013).
62. Malloy, J. N., Paulose, J. K., Li, Y. & Cassone, V. M. Circadian rhythms of gastrointestinal function are regulated by both central and peripheral oscillators. Am. J. Physiol. Gastrointest Liver Physiol. 303, G461-G473 (2012).
63. LeSauter, J., Romero, P., Cascio, M. & Silver, R. Attachment site of grafted SCN influences precision of restored circadian rhythm. J. Biol. Rhythms. 12, 327-338 (1997).
64. Silver, R., LeSauter, J., Tresco, P. A. & Lehman, M. N. A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 382, 810-813 (1996).
65. Lehman, M. N. et al. Circadian rhythmicity restored by neural transplant. Immunocytochemical characterization of the graft and its integration with the host brain. J. Neurosci. 7, 1626-1638 (1987).
66. Zhou, Q. Y. & Cheng, M. Y. Prokineticin 2 and circadian clock output. FEBS J. 272, 5703-5709 (2005).
67. Yoo, S. H. et al. PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc. Natl Acad. Sci. USA 101, 5339-5346 (2004).
68. Yamazaki, S. et al. Resetting central and peripheral circadian oscillators in transgenic rats. Science 288, 682-685 (2000).
69. Balsalobre, A., Damiola, F. & Schibler, U. A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93, 929-937 (1998).
70. Leise, T. L., Wang, C. W., Gitis, P. J. & Welsh, D. K. Persistent cell-autonomous circadian oscillations in fibroblasts revealed by six-week single-cell imaging of PER2::LUC bioluminescence. PLoS ONE 7, e33334 (2012).
71. Klein, D. C. & Moore, R. Y. Pineal N-acetyltransferase and hydroxyindole-O-methyltransferase: control by the retinohypothalamic tract and the suprachiasmatic nucleus. Brain Res. 174, 245-262 (1979).
72. Oster, H. et al. The circadian rhythm of glucocorticoids is regulated by a gating mechanism residing in the adrenal cortical clock. Cell Metab. 4, 163-173 (2006).
73. Son, G. H. et al. Adrenal peripheral clock controls the autonomous circadian rhythm of glucocorticoid by causing rhythmic steroid production. Proc. Natl Acad. Sci. USA 105, 20970-20975 (2008).
74. Allaman-Pillet, N. et al. Circadian regulation of islet genes involved in insulin production and secretion. Mol. Cell. Endocrinol. 226, 59-66 (2004).
75. Marcheva, B. et al. Disruption of the clock components clock and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 466, 627-631 (2010).
76. Sadacca, L. A., Lamia KA, deLemos, A. S., Blum, B. & Weitz, C. J. An intrinsic circadian clock of the pancreas is required for normal insulin release and glucose homeostasis in mice. Diabetologia 54, 120-124 (2011).
77. Knutsson, A., Akerstedt, T., Jonsson, B. & Orth-Gomer, K. Increased risk of ischaemic heart disease in shift workers. Lancet 12, 89-92 (1986).
78. Koller, M. Health risks related to shift work: an example of time-contingent effects of longterm stress. Int. Arch. Occup. Environ. Health 53, 59-75 (1983).
79. Arble, D. M., Ramsey, K. M., Bass, J. & Turek, F. W. Circadian disruption and metabolic disease: findings from animal models. Best Pract. Res. Clin. Endocrinol. Metab. 24, 785-800 (2010).
80. Labyak, S., Lava, S., Turek, F. & Zee, P. Effects of shiftwork on sleep and menstrual function in nurses. Health Care Women Int. 23, 703-714 (2002).
81. Summa, K. C., Vitaterna, M. H. & Turek, F. W. Environmental perturbation of the circadian clock disrupts pregnancy in the mouse. PLoS ONE 7, e37668 (2012).
82. Kennaway, D. J. The role of circadian rhythmicity in reproduction. Hum. Reprod. Update 11, 91-101 (2005).
83. Miller, B. H. et al. Circadian clock mutation disrupts estrous cyclicity and maintenance of pregnancy. Curr. Biol. 14, 1367-1373 (2004).
84. Gamble, K. L., Resuehr, D. & Johnson, C. H. Shift work and circadian dysregulation of reproduction. Front. Endocrinol. (Lausanne) 4, 92 (2013).
85. van den Buuse, M. Circadian rhythms of blood pressure and heart rate in conscious rats: effects of light cycle shift and timed feeding. Physiol. Behav. 68, 9-15 (1999).
86. Durgan, D. J. et al. The circadian clock within the cardiomyocyte is essential for responsiveness of the heart to fatty acids. J. Biol. Chem. 281, 24254-24269 (2006).
87. Davidson, A. J., Castanon-Cervantes, O., Leise, T. L., Molyneux, P. C. & Harrington, M. E. Visualizing jet lag in the mouse suprachiasmatic nucleus and peripheral circadian timing system. Eur. J. Neurosci. 29, 171-180 (2009).
88. Sellix, M. T. et al. Aging differentially affects the re-entrainment response of central and peripheral circadian oscillators. J. Neurosci. 32, 16193-16202 (2012).
89. Tsai, L. L., Tsai, Y. C., Hwang, K., Huang, Y. W. & Tzeng, J. E. Repeated light-dark shifts speed up body weight gain in male F344 rats. Am. J. Physiol. Endocrinol. Metab. 289, E212-E217 (2005).
90. Filipski, E. et al. Circadian disruption accelerates liver carcinogenesis in mice. Mutat. Res. 680, 95-105 (2009).
91. Cambras, T. et al. Circadian desynchronization of core body temperature and sleep stages in the rat. Proc. Natl Acad. Sci. USA 104, 7634-7639 (2007).
92. Castanon-Cervantes, O. et al. Dysregulation of inflammatory responses by chronic circadian disruption. J. Immunol. 185, 5796-5805 (2010).
93. de la Iglesia, H. O., Cambras, T., Schwartz, W. J. & Diez-Noguera, A. Forced desynchronization of dual circadian oscillators within the rat suprachiasmatic nucleus. Curr. Biol. 14, 796-800 (2004).
94. Escobar, C. et al. Circadian disruption leads to loss of homeostasis and disease. Sleep Disord. 2011, 964510 (2011).
95. Bartol-Munier, I., Gourmelen, S., Pevet, P. & Challet, E. Combined effects of high-fat feeding and circadian desynchronization. Int. J. Obes. (Lond.) 30, 60-67 (2006).
96. Salgado-Delgado, R. C. et al. Shift work or food intake during the rest phase promotes metabolic disruption and desynchrony of liver genes in male rats. PLoS ONE 8, e60052 (2013).
97. Bellastella, A. et al. Endocrine secretions under abnormal light-dark cycles and in the blind. Horm. Res. 49, 153-157 (1998).
98. Gibson, E. M., Wang, C., Tjho, S., Khattar, N. & Kriegsfeld, L. J. Experimental 'jet lag' inhibits adult neurogenesis and produces long-term cognitive deficits in female hamsters. PLoS ONE 5, e15267 (2010).
99. Kiessling, S., Eichele, G. & Oster, H. Adrenal glucocorticoids have a key role in circadian resynchronization in a mouse model of jet lag. J. Clin. Invest. 120, 2600-2609 (2010).
100. Vitaterna, M. et al. Mutagenesis and mapping of a mouse gene; clock; essential for circadian behavior. Science 264, 719-725 (1994).
101. Turek, F. et al. Obesity and metabolic syndrome in clock mutant mice. Science 308, 1043-1045 (2005).
102. Kondratov, R. V., Kondratova, A. A., Gorbacheva, V. Y., Vykhovanets, O. V. & Antoch, M. P. Early aging and age-related pathologies in mice deficient in BMAL1, the core component of the circadian clock. Genes Dev. 20, 1868-1873 (2006).
103. Kennaway, D. J., Varcoe, T. J., Voultsios, A. & Boden, M. J. Global loss of BMAL1 expression alters adipose tissue hormones, gene expression and glucose metabolism. PLoS ONE 8, e65255 (2013).
104. Rudic, R. D. et al. BMAL1 and clock, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biol. 2, e377 (2004).
105. Carvas, J. M. et al. Period2 gene mutant mice show compromised insulin-mediated endothelial nitric oxide release and altered glucose homeostasis. Front. Physiol. 3, 337 (2012).
106. Morris, C. J., Aeschbach, D. & Scheer, F. A. Circadian system, sleep and endocrinology. Mol. Cell. Endocrinol. 349, 91-104 (2012).
107. Scheer, F. A., Hilton, M. F., Mantzoros, C. S. & Shea, S. A. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc. Natl Acad. Sci. USA 106, 4453-4458 (2009).
108. Nguyen, J. & Wright, K. P. Jr Influence of weeks of circadian misalignment on leptin levels. Nat. Sci. Sleep 2, 9-18 (2010).
109. Archer, S. N. et al. Mistimed sleep disrupts circadian regulation of the human transcriptome. Proc. Natl Acad. Sci. USA 111, E682-E691 (2014).
110. Leproult, R., Holmbäck, U. & Van Cauter, E. Circadian misalignment augments markers of insulin resistance and inflammation, independently of sleep loss. Diabetes http://dx.doi.org/10.2337/db13-1546.
111. Weibel, L., Spiegel, K., Gronfier, C., Follenius, M. & Brandenberger, G. Twenty-four-hour melatonin and core body temperature rhythms: their adaptation in night workers. Am. J. Physiol. 272, R948-R954 (1997).
112. Boivin, D. B. & James, F. O. Circadian adaptation to night-shift work by judicious light and darkness exposure. J. Biol. Rhythms. 17, 556-567 (2002).
113. Hennig, J., Kieferdorf, P., Moritz, C., Huwe, S. & Netter, P. Changes in cortisol secretion during shiftwork: implications for tolerance to shiftwork? Ergonomics 41, 610-621 (1998).
114. Pietroiusti, A. et al. Incidence of metabolic syndrome among night-shift healthcare workers. Occup. Environ. Med. 67, 54-57 (2010).
115. Lund, J., Arendt, J., Hampton, S. M., English, J. & Morgan, L. M. Postprandial hormone and metabolic responses amongst shift workers in Antarctica. J. Endocrinol. 171, 557-564 (2001).
116. Schiavo-Cardozo, D., Lima, M. M., Pareja, J. C. & Geloneze, B. Appetite-regulating hormones from the upper gut: disrupted control of xenin and ghrelin in night workers. Clin. Endocrinol. (Oxf.) 79, 807-811 (2013).
117. Boivin, D. B., Tremblay, G. M. & James, F. O. Working on atypical schedules. Sleep Med. 8, 578-589 (2007).
118. Foster, R. G. & Wulff, K. The rhythm of rest and excess. Nat. Rev. Neurosci. 6, 407-414 (2005).
119. Knutsson, A., Akerstedt, T., Jonsson, B. G. & Orth-Gomer, K. Increased risk of ischaemic heart disease in shift workers. Lancet 2, 89-92 (1986).
120. Kroenke, C. H. et al. Work characteristics and incidence of type 2 diabetes in women. Am. J. Epidemiol. 165, 175-183 (2007).
121. Ando, H. et al. Clock gene expression in peripheral leucocytes of patients with type 2 diabetes. Diabetologia 52, 329-335 (2009).
122. Boden, G., Chen, X. & Urbain, J. L. Evidence for a circadian rhythm of insulin sensitivity in patients with NIDDM caused by cyclic changes in hepatic glucose production. Diabetes 45, 1044-1050 (1996).
123. Boden, G., Chen, X. & Polansky, M. 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 (1999).
124. Sans-Fuentes, M. A., Diez-Noguera, A. & Cambras, T. Light responses of the circadian system in leptin deficient mice. Physiol. Behav. 99, 487-494 (2010).
125. Danguir, J. Sleep patterns in the genetically obese Zucker rat: effect of acarbose treatment. Am. J. Physiol. 256, R281-R283 (1989).
126. Megirian, D., Dmochowski, J. & Farkas, G. A. Mechanism controlling sleep organization of the obese Zucker rats. J. Appl. Physiol. 84, 253-256 (1998).
127. Kudo, T. et al. Night-time restricted feeding normalises clock genes and Pai-1 gene expression in the db/db mouse liver. Diabetologia 47, 1425-1436 (2004).
128. Laposky, A. D. et al. Altered sleep regulation in leptin-deficient mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R894-R903 (2006).
129. Kohsaka, A. et al. High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab. 6, 414-421 (2007).
130. Pendergast, J. S. et al. High-fat diet acutely affects circadian organisation and eating behavior. Eur. J. Neurosci. 37, 1350-1356 (2013).
131. Shi, S. et al. Circadian clock gene Bmal1 is not essential; functional replacement with its paralog, Bmal2. Curr. Biol. 20, 316-321 (2010).
132. McDearmon, E. L. et al. Dissecting the functions of the mammalian clock protein BMAL1 by tissue-specific rescue in mice. Science 314, 1304-1308 (2006).
133. Hughes, M. E. et al. Harmonics of circadian gene transcription in mammals. PLoS Genet. 5, e1000442 (2009).
134. Hughes, M. E. et al. Brain-specific rescue of clock reveals system-driven transcriptional rhythms in peripheral tissue. PLoS Genet. 8, e1002835 (2012).
135. Damiola, F. et al. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 14, 2950-2961 (2000).
136. Minami, Y., Horikawa, K., Akiyama, M. & Shibata, S. Restricted feeding induces daily expression of clock genes and Pai-1 mRNA in the heart of Clock mutant mice. FEBS Lett. 526, 115-118 (2002).
137. Bray, M. S. et al. Time-of-day-dependent dietary fat consumption influences multiple cardiometabolic syndrome parameters in mice. Int. J. Obes. (Lond.) 34, 1589-1598 (2010).
138. Bray, M. S. et al. Quantitative analysis of lightphase restricted feeding reveals metabolic dyssynchrony in mice. Int. J. Obes. (Lond.) 37, 843-852 (2013).
139. Arble, D. M., Bass, J., Laposky, A. D., Vitaterna, M. H. & Turek, F. W. Circadian timing of food intake contributes to weight gain. Obesity (Silver Spring) 17, 2100-2102 (2009).
140. Fonken, L. K. et al. Light at night increases body mass by shifting the time of food intake. Proc. Natl Acad. Sci. USA 107, 18664-18669 (2010).
141. Hatori, M. et al. Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab. 15, 848-860 (2012).
142. Stunkard, A. J. & Allison, K. C. Two forms of disordered eating in obesity: binge eating and night eating. Int. J. Obes Relat. Metab. Disord. 27, 1-12 (2003).
143. Qin, L. Q. et al. The effects of nocturnal life on endocrine circadian patterns in healthy adults. Life Sci. 73, 2467-2475 (2003).
144. Barclay, J. L. et al. Circadian desynchrony promotes metabolic disruption in a mouse model of shiftwork. PLoS ONE 7, e37150 (2012).
145. Schroeder, A. M. & Colwell, C. S. How to fix a broken clock. Trends Pharmacol. Sci. 34, 605-619 (2013).
146. Hirota, T. et al. High-throughput chemical screen identifies a novel potent modulator of cellular circadian rhythms and reveals CKIα as a clock regulatory kinase. PLoS Biol. 8, e1000559 (2010).
147. Hirota, T. et al. Identification of small molecule activators of cryptochrome. Science 337, 1094-1097 (2012).
148. Solt, L. A. et al. Regulation of circadian behaviour and metabolism by synthetic REV-ERB agonists. Nature 485, 62-68 (2012).
149. Hirota, T. et al. A chemical biology approach reveals period shortening of the mammalian circadian clock by specific inhibition of GSK-3β. Proc. Natl Acad. Sci. USA 105, 20746-20751 (2008).
150. Vougogiannopoulou, K. et al. Soluble 3', 6-substituted indirubins with enhanced selectivity toward glycogen synthase kinase-3 alter circadian period. J. Med. Chem. 51, 6421-6431 (2008).
151. Klingman, K. M., Marsh, E. E, Klerman, E. B., Anderson, E. J. & Hall, J. E. Absence of circadian rhythms of gonadotropin secretion in women. J. Clin. Endocrinol. Metab. 96, 1456-1461 (2011).
152. White, W. B. Importance of blood pressure control over a 24-hour period. J. Manag. Care Pharm. 13, 34-39 (2007).
153. Lee, P. et al. Mild cold exposure modulates fibroblast growth factor 21 (FGF21) diurnal rhythm in humans: relationship between FGF21 levels, lipolysis, and cold-induced thermogenesis. J. Clin. Endocrinol. Metab. 98, E98-E102 (2013).
154. Yu, H. et al. Circadian rhythm of circulating fibroblast growth factor 21 is related to diurnal changes in fatty acids in humans. Clin. Chem. 57, 691-700 (2011).
155. Koutkia, P. et al. Reciprocal changes in endogenous ghrelin and growth hormone during fasting in healthy women. Am. J. Physiol. Endocrinol. Metab. 289, E814-E822 (2005).
156. Natalucci, G., Riedl, S., Gleiss, A., Zidek, T. & Frisch, H. Spontaneous 24-h ghrelin secretion pattern in fasting subjects: Maintenance of a meal-related pattern. Eur. J. Endocrinol. 152, 845-850 (2005).
157. Forsling, M. L. Diurnal rhythms in neurohypophysial function. Exp. Physiol. 85, 179S-186S (2000). Diseases