Skip to main content

The role of the circadian clock system in nutrition and metabolism

  • Felino R. Cagampang (a1) and Kimberley D. Bruce (a1)

Mammals have an endogenous timing system in the suprachiasmatic nuclei (SCN) of the hypothalamic region of the brain. This internal clock system is composed of an intracellular feedback loop that drives the expression of molecular components and their constitutive protein products to oscillate over a period of about 24 h (hence the term ‘circadian’). These circadian oscillations bring about rhythmic changes in downstream molecular pathways and physiological processes such as those involved in nutrition and metabolism. It is now emerging that the molecular components of the clock system are also found within the cells of peripheral tissues, including the gastrointestinal tract, liver and pancreas. The present review examines their role in regulating nutritional and metabolic processes. In turn, metabolic status and feeding cycles are able to feed back onto the circadian clock in the SCN and in peripheral tissues. This feedback mechanism maintains the integrity and temporal coordination between various components of the circadian clock system. Thus, alterations in environmental cues could disrupt normal clock function, which may have profound effects on the health and well-being of an individual.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      The role of the circadian clock system in nutrition and metabolism
      Available formats
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      The role of the circadian clock system in nutrition and metabolism
      Available formats
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      The role of the circadian clock system in nutrition and metabolism
      Available formats
Corresponding author
*Corresponding author: Dr F. R. Cagampang, email
Hide All
1Panda, S & Hogenesch, JB (2004) It's all in the timing: many clocks, many outputs. J Biol Rhythms 19, 374387.
2Roenneberg, T, Kumar, CJ & Merrow, M (2007) The human circadian clock entrains to sun time. Curr Biol 17, R44R45.
3Rana, S & Mahmood, S (2010) Circadian rhythm and its role in malignancy. J Circadian Rhythms 8, 3.
4Rosenwasser, AM (2010) Circadian clock genes: non-circadian roles in sleep, addiction, and psychiatric disorders? Neurosci Biobehav Rev 34, 12491255.
5Mahoney, MM (2010) Shift work, jet lag, and female reproduction. Int J Endocrinol 2010, 813764.
6Takeda, N & Maemura, K (2010) Circadian clock and vascular disease. Hypertens Res 33, 645651.
7Froy, O (2011) Circadian rhythms, aging, and life span in mammals. Physiology (Bethesda) 26, 225235.
8Jung-Hynes, B, Reiter, RJ & Ahmad, N (2010) Sirtuins, melatonin and circadian rhythms: building a bridge between aging and cancer. J Pineal Res 48, 919.
9Krishnan, N, Kretzschmar, D, Rakshit, K, et al. (2009) The circadian clock gene period extends healthspan in aging Drosophila melanogaster. Aging (Albany NY) 1, 937948.
10Ramsey, KM & Bass, J (2009) Obeying the clock yields benefits for metabolism. Proc Natl Acad Sci U S A 106, 40694070.
11Dibner, C, Schibler, U & Albrecht, U (2010) The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 72, 517549.
12Rosbash, M (2009) The implications of multiple circadian clock origins. PLoS Biol 7, e62.
13Lowrey, PL & Takahashi, JS (2011) Genetics of circadian rhythms in mammalian model organisms. Adv Genet 74, 175230.
14Doi, M, Hirayama, J & Sassone-Corsi, P (2006) Circadian regulator CLOCK is a histone acetyltransferase. Cell 125, 497508.
15Eide, EJ, Woolf, MF, Kang, H, et al. (2005) Control of mammalian circadian rhythm by CKIepsilon-regulated proteasome-mediated PER2 degradation. Mol Cell Biol 25, 27952807.
16Harms, E, Kivimae, S, Young, MW, et al. (2004) Posttranscriptional and posttranslational regulation of clock genes. J Biol Rhythms 19, 361373.
17Preitner, N, Damiola, F, Lopez-Molina, L, et al. (2002) The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110, 251260.
18Sato, TK, Panda, S, Miraglia, LJ, et al. (2004) A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron 43, 527537.
19Ueda, HR, Hayashi, S, Chen, W, et al. (2005) System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat Genet 37, 187192.
20Kalsbeek, A, Palm, IF, La Fleur, SE, et al. (2006) SCN outputs and the hypothalamic balance of life. J Biol Rhythms 21, 458469.
21Lowrey, PL & Takahashi, JS (2004) Mammalian circadian biology: elucidating genome-wide levels of temporal organization. Annu Rev Genomics Hum Genet 5, 407441.
22Takahashi, JS, Hong, HK, Ko, CH, et al. (2008) The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat Rev Genet 9, 764775.
23Mohawk, JA & Takahashi, JS (2011) Cell autonomy and synchrony of suprachiasmatic nucleus circadian oscillators. Trends Neurosci 34, 349358.
24Stephan, FK & Nunez, AA (1977) Elimination of circadian rhythms in drinking, activity, sleep, and temperature by isolation of the suprachiasmatic nuclei. Behav Biol 20, 161.
25Silver, R, LeSauter, J, Tresco, PA, et al. (1996) A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 382, 810813.
26Aguilar-Roblero, R, Morin, LP & Moore, RY (1994) Morphological correlates of circadian rhythm restoration induced by transplantation of the suprachiasmatic nucleus in hamsters. Exp Neurol 130, 250260.
27Maury, E, Ramsey, KM & Bass, J (2010) Circadian rhythms and metabolic syndrome: from experimental genetics to human disease. Circ Res 106, 447462.
28Stokkan, KA, van Oort, BE, Tyler, NJ, et al. (2007) Adaptations for life in the Arctic: evidence that melatonin rhythms in reindeer are not driven by a circadian oscillator but remain acutely sensitive to environmental photoperiod. J Pineal Res 43, 289293.
29Albrecht, U & Eichele, G (2003) The mammalian circadian clock. Curr Opin Genet Dev 13, 271277.
30Peirson, S & Foster, RG (2006) Melanopsin: another way of signaling light. Neuron 49, 331339.
31Reppert, SM & Weaver, DR (2002) Coordination of circadian timing in mammals. Nature 418, 935941.
32Peirson, SN, Butler, JN, Duffield, GE, et al. (2006) Comparison of clock gene expression in SCN, retina, heart, and liver of mice. Biochem Biophys Res Commun 351, 800807.
33Young, ME, Razeghi, P & Taegtmeyer, H (2001) Clock genes in the heart: characterization and attenuation with hypertrophy. Circ Res 88, 11421150.
34Davidson, AJ, Castanon-Cervantes, O & Stephan, FK (2004) Daily oscillations in liver function: diurnal vs circadian rhythmicity. Liver Int 24, 179186.
35Konturek, PC, Brzozowski, T & Konturek, SJ (2011) Gut clock: implication of circadian rhythms in the gastrointestinal tract. J Physiol Pharmacol 62, 139150.
36Hoogerwerf, WA, Hellmich, HL, Cornelissen, G, et al. (2007) Clock gene expression in the murine gastrointestinal tract: endogenous rhythmicity and effects of a feeding regimen. Gastroenterology 133, 12501260.
37Marcheva, B, Ramsey, KM, Buhr, ED, et al. (2010) Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 466, 627631.
38Sadacca, LA, Lamia, KA, deLemos, AS, et al. (2011) An intrinsic circadian clock of the pancreas is required for normal insulin release and glucose homeostasis in mice. Diabetologia 54, 120124.
39Lee, C, Etchegaray, JP, Cagampang, FR, et al. (2001) Posttranslational mechanisms regulate the mammalian circadian clock. Cell 107, 855867.
40Yoo, SH, Yamazaki, S, Lowrey, PL, et al. (2004) PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci U S A 101, 53395346.
41Kreier, F, Kalsbeek, A, Ruiter, M, et al. (2003) Central nervous determination of food storage – a daily switch from conservation to expenditure: implications for the metabolic syndrome. Eur J Pharmacol 480, 5165.
42Li, JD, Hu, WP, Boehmer, L, et al. (2006) Attenuated circadian rhythms in mice lacking the prokineticin 2 gene. J Neurosci 26, 1161511623.
43Prosser, HM, Bradley, A, Chesham, JE, et al. (2007) Prokineticin receptor 2 (Prokr2) is essential for the regulation of circadian behavior by the suprachiasmatic nuclei. Proc Natl Acad Sci U S A 104, 648653.
44Kalsbeek, A, Fliers, E, Hofman, MA, et al. (2010) Vasopressin and the output of the hypothalamic biological clock. J Neuroendocrinol 22, 362372.
45Kalsbeek, A, Buijs, RM, van Heerikhuize, JJ, et al. (1992) Vasopressin-containing neurons of the suprachiasmatic nuclei inhibit corticosterone release. Brain Res 580, 6267.
46Kraves, S & Weitz, CJ (2006) A role for cardiotrophin-like cytokine in the circadian control of mammalian locomotor activity. Nat Neurosci 9, 212219.
47Kalsbeek, A & Buijs, RM (1992) Peptidergic transmitters of the suprachiasmatic nuclei and the control of circadian rhythmicity. Prog Brain Res 92, 321333.
48Yi, CX, Serlie, MJ, Ackermans, MT, et al. (2009) A major role for perifornical orexin neurons in the control of glucose metabolism in rats. Diabetes 58, 19982005.
49Yi, CX, Sun, N, Ackermans, MT, et al. (2010) Pituitary adenylate cyclase-activating polypeptide stimulates glucose production via the hepatic sympathetic innervation in rats. Diabetes 59, 15911600.
50Li, X, Sankrithi, N & Davis, FC (2002) Transforming growth factor-alpha is expressed in astrocytes of the suprachiasmatic nucleus in hamster: role of glial cells in circadian clocks. Neuroreport 13, 21432147.
51Moore, RY (1996) Neural control of the pineal gland. Behav Brain Res 73, 125130.
52Engel, L, Lorenzkowski, V, Langer, C, et al. (2005) The photoperiod entrains the molecular clock of the rat pineal. Eur J Neurosci 21, 22972304.
53Kalsbeek, A, Foppen, E, Schalij, I, et al. (2008) Circadian control of the daily plasma glucose rhythm: an interplay of GABA and glutamate. PLoS One 3, e3194.
54Buijs, RM, La Fleur, SE, Wortel, J, et al. (2003) The suprachiasmatic nucleus balances sympathetic and parasympathetic output to peripheral organs through separate preautonomic neurons. J Comp Neurol 464, 3648.
55Cailotto, C, La Fleur, SE, van, HC, et al. (2005) The suprachiasmatic nucleus controls the daily variation of plasma glucose via the autonomic output to the liver: are the clock genes involved? Eur J Neurosci 22, 25312540.
56Kalsbeek, A, Ruiter, M, La Fleur, SE, et al. (2006) The hypothalamic clock and its control of glucose homeostasis. Prog Brain Res 153, 283307.
57Kreier, F, Fliers, E, Voshol, PJ, et al. (2002) Selective parasympathetic innervation of subcutaneous and intra-abdominal fat – functional implications. J Clin Invest 110, 12431250.
58Kalsbeek, A, Fliers, E, Romijn, JA, et al. (2001) The suprachiasmatic nucleus generates the diurnal changes in plasma leptin levels. Endocrinology 142, 26772685.
59Kobayashi, H, Oishi, K, Hanai, S, et al. (2004) Effect of feeding on peripheral circadian rhythms and behaviour in mammals. Genes Cells 9, 857864.
60Schibler, U, Ripperger, J & Brown, SA (2003) Peripheral circadian oscillators in mammals: time and food. J Biol Rhythms 18, 250260.
61Brown, SA, Zumbrunn, G, Fleury-Olela, F, et al. (2002) Rhythms of mammalian body temperature can sustain peripheral circadian clocks. Curr Biol 12, 15741583.
62Buxton, OM, Lee, CW, L'Hermite-Baleriaux, M, et al. (2003) Exercise elicits phase shifts and acute alterations of melatonin that vary with circadian phase. Am J Physiol Regul Integr Comp Physiol 284, R714R724.
63Stokkan, KA, Yamazaki, S, Tei, H, et al. (2001) Entrainment of the circadian clock in the liver by feeding. Science 291, 490493.
64van Someren, EJ & Riemersma-van der Lek, RF (2007) Live to the rhythm, slave to the rhythm. Sleep Med Rev 11, 465484.
65Liu, AC, Welsh, DK, Ko, CH, et al. (2007) Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell 129, 605616.
66Guo, H, Brewer, JM, Lehman, MN, et al. (2006) Suprachiasmatic regulation of circadian rhythms of gene expression in hamster peripheral organs: effects of transplanting the pacemaker. J Neurosci 26, 64066412.
67Kornmann, B, Schaad, O, Bujard, H, et al. (2007) System-driven and oscillator-dependent circadian transcription in mice with a conditionally active liver clock. PLoS Biol 5, e34.
68Hirota, T & Fukada, Y (2004) Resetting mechanism of central and peripheral circadian clocks in mammals. Zoolog Sci 21, 359368.
69Escobar, C, Cailotto, C, Angeles-Castellanos, M, et al. (2009) Peripheral oscillators: the driving force for food-anticipatory activity. Eur J Neurosci 30, 16651675.
70Mistlberger, RE (2011) Neurobiology of food anticipatory circadian rhythms. Physiol Behav 104, 535545.
71Knutsson, A & Boggild, H (2010) Gastrointestinal disorders among shift workers. Scand J Work Environ Health 36, 8595.
72Hoogerwerf, WA (2009) Role of biological rhythms in gastrointestinal health and disease. Rev Endocr Metab Disord 10, 293300.
73Szosland, D (2010) Shift work and metabolic syndrome, diabetes mellitus and ischaemic heart disease. Int J Occup Med Environ Health 23, 287291.
74Scheer, FA, Hilton, MF, Mantzoros, CS, et al. (2009) Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc Natl Acad Sci U S A 106, 44534458.
75Wynne, K, Stanley, S, McGowan, B, et al. (2005) Appetite control. J Endocrinol 184, 291318.
76Funahashi, H, Takenoya, F, Guan, JL, et al. (2003) Hypothalamic neuronal networks and feeding-related peptides involved in the regulation of feeding. Anat Sci Int 78, 123138.
77Valassi, E, Scacchi, M & Cavagnini, F (2008) Neuroendocrine control of food intake. Nutr Metab Cardiovasc Dis 18, 158168.
78Lu, XY, Shieh, KR, Kabbaj, M, et al. (2002) Diurnal rhythm of agouti-related protein and its relation to corticosterone and food intake. Endocrinology 143, 39053915.
79Stutz, AM, Staszkiewicz, J, Ptitsyn, A, et al. (2007) Circadian expression of genes regulating food intake. Obesity (Silver Spring) 15, 607615.
80Xu, B, Kalra, PS, Farmerie, WG, et al. (1999) Daily changes in hypothalamic gene expression of neuropeptide Y, galanin, proopiomelanocortin, and adipocyte leptin gene expression and secretion: effects of food restriction. Endocrinology 140, 28682875.
81Sindelar, DK, Palmiter, RD, Woods, SC, et al. (2005) Attenuated feeding responses to circadian and palatability cues in mice lacking neuropeptide Y. Peptides 26, 25972602.
82Feillet, CA, Mendoza, J, Albrecht, U, et al. (2008) Forebrain oscillators ticking with different clock hands. Mol Cell Neurosci 37, 209221.
83Wyse, CA & Coogan, AN (2010) Impact of aging on diurnal expression patterns of CLOCK and BMAL1 in the mouse brain. Brain Res 1337, 2131.
84Asai, M, Yoshinobu, Y, Kaneko, S, et al. (2001) Circadian profile of Per gene mRNA expression in the suprachiasmatic nucleus, paraventricular nucleus, and pineal body of aged rats. J Neurosci Res 66, 11331139.
85Abe, M, Herzog, ED, Yamazaki, S, et al. (2002) Circadian rhythms in isolated brain regions. J Neurosci 22, 350356.
86Kriegsfeld, LJ, Korets, R & Silver, R (2003) Expression of the circadian clock gene Period 1 in neuroendocrine cells: an investigation using mice with a Per1::GFP transgene. Eur J Neurosci 17, 212220.
87Guilding, C, Hughes, AT, Brown, TM, et al. (2009) A riot of rhythms: neuronal and glial circadian oscillators in the mediobasal hypothalamus. Mol Brain 2, 28.
88Aschoff, J, von, GC, Wildgruber, C, et al. (1986) Meal timing in humans during isolation without time cues. J Biol Rhythms 1, 151162.
89Fonken, LK, Workman, JL, Walton, JC, et al. (2010) Light at night increases body mass by shifting the time of food intake. Proc Natl Acad Sci U S A 107, 1866418669.
90Lowden, A, Moreno, C, Holmback, U, et al. (2010) Eating and shift work – effects on habits, metabolism and performance. Scand J Work Environ Health 36, 150162.
91Morikawa, Y, Nakagawa, H, Miura, K, et al. (2007) Effect of shift work on body mass index and metabolic parameters. Scand J Work Environ Health 33, 4550.
92Kalra, SP, Bagnasco, M, Otukonyong, EE, et al. (2003) Rhythmic, reciprocal ghrelin and leptin signaling: new insight in the development of obesity. Regul Pept 111, 111.
93Lecoultre, V, Ravussin, E & Redman, LM (2011) The fall in leptin concentration is a major determinant of the metabolic adaptation induced by caloric restriction independently of the changes in leptin circadian rhythms. J Clin Endocrinol Metab 96, E1512E1516.
94Wong, ML, Licinio, J, Yildiz, BO, et al. (2004) Simultaneous and continuous 24-hour plasma and cerebrospinal fluid leptin measurements: dissociation of concentrations in central and peripheral compartments. J Clin Endocrinol Metab 89, 258265.
95Yildiz, BO, Suchard, MA, Wong, ML, et al. (2004) Alterations in the dynamics of circulating ghrelin, adiponectin, and leptin in human obesity. Proc Natl Acad Sci U S A 101, 1043410439.
96Cinti, S, Matteis, RD, Pico, C, et al. (2000) Secretory granules of endocrine and chief cells of human stomach mucosa contain leptin. Int J Obes Relat Metab Disord 24, 789793.
97Bado, A, Levasseur, S, Attoub, S, et al. (1998) The stomach is a source of leptin. Nature 394, 790793.
98Cinti, S, De, MR, Ceresi, E, et al. (2001) Leptin in the human stomach. Gut 49, 155.
99Kojima, M & Kangawa, K (2002) Ghrelin, an orexigenic signaling molecule from the gastrointestinal tract. Curr Opin Pharmacol 2, 665668.
100Cowley, MA, Smith, RG, Diano, S, et al. (2003) The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuit regulating energy homeostasis. Neuron 37, 649661.
101Chen, HY, Trumbauer, ME, Chen, AS, et al. (2004) Orexigenic action of peripheral ghrelin is mediated by neuropeptide Y and agouti-related protein. Endocrinology 145, 26072612.
102Hagemann, D, Meier, JJ, Gallwitz, B, et al. (2003) Appetite regulation by ghrelin – a novel neuro-endocrine gastric peptide hormone in the gut-brain-axis. Z Gastroenterol 41, 929936.
103Yi, CX, Challet, E, Pevet, P, et al. (2008) A circulating ghrelin mimetic attenuates light-induced phase delay of mice and light-induced Fos expression in the suprachiasmatic nucleus of rats. Eur J Neurosci 27, 19651972.
104Yannielli, PC, Molyneux, PC, Harrington, ME, et al. (2007) Ghrelin effects on the circadian system of mice. J Neurosci 27, 28902895.
105Cummings, DE, Purnell, JQ, Frayo, RS, et al. (2001) A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes 50, 17141719.
106Schmid, SM, Hallschmid, M, Jauch-Chara, K, et al. (2008) A single night of sleep deprivation increases ghrelin levels and feelings of hunger in normal-weight healthy men. J Sleep Res 17, 331334.
107Tschop, M, Weyer, C, Tataranni, PA, et al. (2001) Circulating ghrelin levels are decreased in human obesity. Diabetes 50, 707709.
108Otto, B, Cuntz, U, Fruehauf, E, et al. (2001) Weight gain decreases elevated plasma ghrelin concentrations of patients with anorexia nervosa. Eur J Endocrinol 145, 669673.
109Sanchez, J, Oliver, P, Pico, C, et al. (2004) Diurnal rhythms of leptin and ghrelin in the systemic circulation and in the gastric mucosa are related to food intake in rats. Pflugers Arch 448, 500506.
110Tempel, DL & Leibowitz, SF (1989) PVN steroid implants: effect on feeding patterns and macronutrient selection. Brain Res Bull 23, 553560.
111Leibowitz, SF (1992) Neurochemical-neuroendocrine systems in the brain controlling macronutrient intake and metabolism. Trends Neurosci 15, 491497.
112Lax, P, Larue-Achagiotis, C, Martel, P, et al. (1998) Repeated short-fasting modifies the macronutrient self-selection pattern in rats. Physiol Behav 65, 6976.
113Westerterp-Plantenga, MS, Ijedema, MJ & Wijckmans-Duijsens, NE (1996) The role of macronutrient selection in determining patterns of food intake in obese and non-obese women. Eur J Clin Nutr 50, 580591.
114Dos Santos, ML, Aragon, FF, Padovani, CR, et al. (2006) Daytime variations in glucose tolerance in people with impaired glucose tolerance. Diabetes Res Clin Pract 74, 257262.
115Sladek, M, Rybova, M, Jindrakova, Z, et al. (2007) Insight into the circadian clock within rat colonic epithelial cells. Gastroenterology 133, 12401249.
116Polidarova, L, Sladek, M, Sotak, M, et al. (2011) Hepatic, duodenal, and colonic circadian clocks differ in their persistence under conditions of constant light and in their entrainment by restricted feeding. Chronobiol Int 28, 204215.
117Bjarnason, GA & Jordan, R (2002) Rhythms in human gastrointestinal mucosa and skin. Chronobiol Int 19, 129140.
118Scheving, LA & Russell, WE (2007) It's about time: clock genes unveiled in the gut. Gastroenterology 133, 13731376.
119Polidarova, L, Sotak, M, Sladek, M, et al. (2009) Temporal gradient in the clock gene and cell-cycle checkpoint kinase Wee1 expression along the gut. Chronobiol Int 26, 607620.
120Hoogerwerf, WA (2006) Biologic clocks and the gut. Curr Gastroenterol Rep 8, 353359.
121Keller, J, Groger, G, Cherian, L, et al. (2001) Circadian coupling between pancreatic secretion and intestinal motility in humans. Am J Physiol Gastrointest Liver Physiol 280, G273G278.
122Moore, JG & Englert, E Jr (1970) Circadian rhythm of gastric acid secretion in man. Nature 226, 12611262.
123Goo, RH, Moore, JG, Greenberg, E, et al. (1987) Circadian variation in gastric emptying of meals in humans. Gastroenterology 93, 515518.
124Moore, JG, Larsen, KR, Barattini, P, et al. (1994) Asynchrony in circadian rhythms of gastric function in the rat. A model for gastric mucosal injury. Dig Dis Sci 39, 16191624.
125Fatima, J, Iqbal, CW, Houghton, SG, et al. (2009) Hexose transporter expression and function in mouse small intestine: role of diurnal rhythm. J Gastrointest Surg 13, 634641.
126Rhoads, DB, Rosenbaum, DH, Unsal, H, et al. (1998) Circadian periodicity of intestinal Na+/glucose cotransporter 1 mRNA levels is transcriptionally regulated. J Biol Chem 273, 95109516.
127Pan, X, Terada, T, Okuda, M, et al. (2004) The diurnal rhythm of the intestinal transporters SGLT1 and PEPT1 is regulated by the feeding conditions in rats. J Nutr 134, 22112215.
128Pan, X, Terada, T, Irie, M, et al. (2002) Diurnal rhythm of H+-peptide cotransporter in rat small intestine. Am J Physiol Gastrointest Liver Physiol 283, G57G64.
129Saito, H, Terada, T, Shimakura, J, et al. (2008) Regulatory mechanism governing the diurnal rhythm of intestinal H+/peptide cotransporter 1 (PEPT1). Am J Physiol Gastrointest Liver Physiol 295, G395G402.
130Pan, X & Hussain, MM (2009) Clock is important for food and circadian regulation of macronutrient absorption in mice. J Lipid Res 50, 18001813.
131Pan, X, Terada, T, Okuda, M, et al. (2003) Altered diurnal rhythm of intestinal peptide transporter by fasting and its effects on the pharmacokinetics of ceftibuten. J Pharmacol Exp Ther 307, 626632.
132Kumar, D, Wingate, D & Ruckebusch, Y (1986) Circadian variation in the propagation velocity of the migrating motor complex. Gastroenterology 91, 926930.
133Rao, SS, Sadeghi, P, Beaty, J, et al. (2001) Ambulatory 24-h colonic manometry in healthy humans. Am J Physiol Gastrointest Liver Physiol 280, G629G639.
134Vener, KJ, Szabo, S & Moore, JG (1989) The effect of shift work on gastrointestinal (GI) function: a review. Chronobiologia 16, 421439.
135Storch, KF, Lipan, O, Leykin, I, et al. (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417, 7883.
136Reddy, AB, Karp, NA, Maywood, ES, et al. (2006) Circadian orchestration of the hepatic proteome. Curr Biol 16, 11071115.
137Turek, FW & Allada, R (2002) Liver has rhythm. Hepatology 35, 743745.
138Panda, S, Antoch, MP, Miller, BH, et al. (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109, 307320.
139Akhtar, RA, Reddy, AB, Maywood, ES, et al. (2002) Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr Biol 12, 540550.
140Gachon, F, Olela, FF, Schaad, O, et al. (2006) The circadian PAR-domain basic leucine zipper transcription factors DBP, TEF, and HLF modulate basal and inducible xenobiotic detoxification. Cell Metab 4, 2536.
141Kalsbeek, A, Yi, CX, La Fleur, SE, et al. (2010) The hypothalamic clock and its control of glucose homeostasis. Trends Endocrinol Metab 21, 402410.
142Simon, C, Weibel, L & Brandenberger, G (2000) Twenty-four-hour rhythms of plasma glucose and insulin secretion rate in regular night workers. Am J Physiol Endocrinol Metab 278, E413E420.
143La Fleur, SE, Kalsbeek, A, Wortel, J, et al. (2000) Polysynaptic neural pathways between the hypothalamus, including the suprachiasmatic nucleus, and the liver. Brain Res 871, 5056.
144La Fleur, SE, Kalsbeek, A, Wortel, J, et al. (2001) A daily rhythm in glucose tolerance: a role for the suprachiasmatic nucleus. Diabetes 50, 12371243.
145Lee, A, Ader, M, Bray, GA, et al. (1992) Diurnal variation in glucose tolerance. Cyclic suppression of insulin action and insulin secretion in normal-weight, but not obese, subjects. Diabetes 41, 750759.
146Carroll, KF & Nestel, PJ (1973) Diurnal variation in glucose tolerance and in insulin secretion in man. Diabetes 22, 333348.
147Cuesta, M, Clesse, D, Pevet, P, et al. (2009) From daily behavior to hormonal and neurotransmitters rhythms: comparison between diurnal and nocturnal rat species. Horm Behav 55, 338347.
148Maouyo, D, Sarfati, P, Guan, D, et al. (1993) Circadian rhythm of exocrine pancreatic secretion in rats: major and minor cycles. Am J Physiol 264, G792G800.
149Langlois, A & Morisset, J (1991) Effects of feeding, fasting, and caerulein treatment on ornithine decarboxylase in rat pancreas. Pancreas 6, 534541.
150Muhlbauer, E, Wolgast, S, Finckh, U, et al. (2004) Indication of circadian oscillations in the rat pancreas. FEBS Lett 564, 9196.
151Peschke, E & Peschke, D (1998) Evidence for a circadian rhythm of insulin release from perifused rat pancreatic islets. Diabetologia 41, 10851092.
152Keller, J & Layer, P (2002) Circadian pancreatic enzyme pattern and relationship between secretory and motor activity in fasting humans. J Appl Physiol 93, 592600.
153Boden, G, Chen, X & Polansky, M (1999) Disruption of circadian insulin secretion is associated with reduced glucose uptake in first-degree relatives of patients with type 2 diabetes. Diabetes 48, 21822188.
154Stephan, FK (2002) The ‘other’ circadian system: food as a Zeitgeber. J Biol Rhythms 17, 284292.
155Comperatore, CA & Stephan, FK (1987) Entrainment of duodenal activity to periodic feeding. J Biol Rhythms 2, 227242.
156Boulamery-Velly, A, Simon, N, Vidal, J, et al. (2005) Effects of three-hour restricted food access during the light period on circadian rhythms of temperature, locomotor activity, and heart rate in rats. Chronobiol Int 22, 489498.
157Miki, H, Yano, M, Iwanaga, H, et al. (2003) Total parenteral nutrition entrains the central and peripheral circadian clocks. Neuroreport 14, 14571461.
158Mistlberger, R & Rusak, B (1987) Palatable daily meals entrain anticipatory activity rhythms in free-feeding rats: dependence on meal size and nutrient content. Physiol Behav 41, 219226.
159Hsu, CT, Patton, DF, Mistlberger, RE, et al. (2010) Palatable meal anticipation in mice. PLoS One 5, e12903.
160Storch, KF & Weitz, CJ (2009) Daily rhythms of food-anticipatory behavioral activity do not require the known circadian clock. Proc Natl Acad Sci U S A 106, 68086813.
161Stephan, FK (1989) Entrainment of activity to multiple feeding times in rats with suprachiasmatic lesions. Physiol Behav 46, 489497.
162Mieda, M, Williams, SC, Richardson, JA, et al. (2006) The dorsomedial hypothalamic nucleus as a putative food-entrainable circadian pacemaker. Proc Natl Acad Sci U S A 103, 1215012155.
163Gooley, JJ, Schomer, A & Saper, CB (2006) The dorsomedial hypothalamic nucleus is critical for the expression of food-entrainable circadian rhythms. Nat Neurosci 9, 398407.
164Fuller, PM, Lu, J & Saper, CB (2008) Differential rescue of light- and food-entrainable circadian rhythms. Science 320, 10741077.
165Vieira, E, Marroqui, L, Batista, TM, et al. (2012) The clock gene Rev-erbalpha regulates pancreatic beta-cell function: modulation by leptin and high-fat diet. Endocrinology 153, 592601.
166Hsieh, MC, Yang, SC, Tseng, HL, et al. (2010) Abnormal expressions of circadian-clock and circadian clock-controlled genes in the livers and kidneys of long-term, high-fat-diet-treated mice. Int J Obes (Lond) 34, 227239.
167Kohsaka, A, Laposky, AD, Ramsey, KM, et al. (2007) High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab 6, 414421.
168Turek, FW, Joshu, C, Kohsaka, A, et al. (2005) Obesity and metabolic syndrome in circadian Clock mutant mice. Science 308, 10431045.
169Rudic, RD, McNamara, P, Curtis, AM, et al. (2004) BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biol 2, e377.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Altmetric attention score

Full text views

Total number of HTML views: 70
Total number of PDF views: 321 *
Loading metrics...

Abstract views

Total abstract views: 672 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 22nd March 2018. This data will be updated every 24 hours.