Meal Timing Regulates the Human Circadian System

Current Biology

Volumn 27, Issue 12, 2017, Pages 1768-1775.e3

  Wehrens, Sophie M T ^a   Christou, Skevoulla ^a   Isherwood, Cheryl ^a   Middleton, Benita ^a   Gibbs, Michelle A ^a   Archer, Simon N ^a   Skene, Debra J ^a   Johnston, Jonathan D ^a  

^a UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

actigraphy; chrononutrition; clock gene; food timing; glucose homeostasis; jet lag; meal timing; peripheral clocks; shift work; white adipose tissue

Indexed keywords

BIOLOGICAL RHYTHM; CIRCADIAN RHYTHM; EATING; HUMAN; MALE; TIME FACTOR;

BIOLOGICAL CLOCKS; CIRCADIAN RHYTHM; EATING; HUMANS; MALE; TIME FACTORS;

EID: 85020089463     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2017.04.059     Document Type: Article

References (53)

1. Bass, J., Circadian topology of metabolism. Nature 491 (2012), 348–356.
2. Johnston, J.D., Ordovás, J.M., Scheer, F.A., Turek, F.W., Circadian rhythms, metabolism, and chrononutrition in rodents and humans. Adv. Nutr. 7 (2016), 399–406.
3. Schibler, U., Gotic, I., Saini, C., Gos, P., Curie, T., Emmenegger, Y., Sinturel, F., Gosselin, P., Gerber, A., Fleury-Olela, F., et al. Clock-talk: interactions between central and peripheral circadian oscillators in mammals. Cold Spring Harb. Symp. Quant. Biol. 80 (2015), 223–232.
4. Roenneberg, T., Merrow, M., The circadian clock and human health. Curr. Biol. 26 (2016), R432–R443.
5. Potter, G.D., Skene, D.J., Arendt, J., Cade, J.E., Grant, P.J., Hardie, L.J., Circadian rhythm and sleep disruption: causes, metabolic consequences, and countermeasures. Endocr. Rev. 37 (2016), 584–608.
6. Lucas, R.J., Peirson, S.N., Berson, D.M., Brown, T.M., Cooper, H.M., Czeisler, C.A., Figueiro, M.G., Gamlin, P.D., Lockley, S.W., O'Hagan, J.B., et al. Measuring and using light in the melanopsin age. Trends Neurosci. 37 (2014), 1–9.
7. Lockley, S.W., Arendt, J., Skene, D.J., Visual impairment and circadian rhythm disorders. Dialogues Clin. Neurosci. 9 (2007), 301–314.
8. Damiola, F., Le Minh, N., Preitner, N., Kornmann, B., Fleury-Olela, F., Schibler, U., Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 14 (2000), 2950–2961.
9. Stokkan, K.A., Yamazaki, S., Tei, H., Sakaki, Y., Menaker, M., Entrainment of the circadian clock in the liver by feeding. Science 291 (2001), 490–493.
10. Mendoza, J., Graff, C., Dardente, H., Pevet, P., Challet, E., Feeding cues alter clock gene oscillations and photic responses in the suprachiasmatic nuclei of mice exposed to a light/dark cycle. J. Neurosci. 25 (2005), 1514–1522.
11. Johnston, J.D., Physiological responses to food intake throughout the day. Nutr. Res. Rev. 27 (2014), 107–118.
12. Van Cauter, E., Polonsky, K.S., Scheen, A.J., Roles of circadian rhythmicity and sleep in human glucose regulation. Endocr. Rev. 18 (1997), 716–738.
13. Morgan, L., Hampton, S., Gibbs, M., Arendt, J., Circadian aspects of postprandial metabolism. Chronobiol. Int. 20 (2003), 795–808.
14. 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 (2009), 4453–4458.
15. Arble, D.M., Bass, J., Behn, C.D., Butler, M.P., Challet, E., Czeisler, C., Depner, C.M., Elmquist, J., Franken, P., Grandner, M.A., et al. Impact of sleep and circadian disruption on energy balance and diabetes: a summary of workshop discussions. Sleep 38 (2015), 1849–1860.
16. Otway, D.T., Mäntele, S., Bretschneider, S., Wright, J., Trayhurn, P., Skene, D.J., Robertson, M.D., Johnston, J.D., Rhythmic diurnal gene expression in human adipose tissue from individuals who are lean, overweight, and type 2 diabetic. Diabetes 60 (2011), 1577–1581.
17. Mäntele, S., Otway, D.T., Middleton, B., Bretschneider, S., Wright, J., Robertson, M.D., Skene, D.J., Johnston, J.D., Daily rhythms of plasma melatonin, but not plasma leptin or leptin mRNA, vary between lean, obese and type 2 diabetic men. PLoS ONE, 7, 2012, e37123.
18. Archer, S.N., Viola, A.U., Kyriakopoulou, V., von Schantz, M., Dijk, D.J., Inter-individual differences in habitual sleep timing and entrained phase of endogenous circadian rhythms of BMAL1, PER2 and PER3 mRNA in human leukocytes. Sleep 31 (2008), 608–617.
19. Duffy, J.F., Dijk, D.J., Getting through to circadian oscillators: why use constant routines?. J. Biol. Rhythms 17 (2002), 4–13.
20. Scheer, F.A., Morris, C.J., Shea, S.A., The internal circadian clock increases hunger and appetite in the evening independent of food intake and other behaviors. Obesity (Silver Spring) 21 (2013), 421–423.
21. Sargent, C., Zhou, X., Matthews, R.W., Darwent, D., Roach, G.D., Daily rhythms of hunger and satiety in healthy men during one week of sleep restriction and circadian misalignment. Int. J. Environ. Res. Public Health, 13, 2016, 170.
22. Shea, S.A., Hilton, M.F., Orlova, C., Ayers, R.T., Mantzoros, C.S., Independent circadian and sleep/wake regulation of adipokines and glucose in humans. J. Clin. Endocrinol. Metab. 90 (2005), 2537–2544.
23. Kräuchi, K., Cajochen, C., Werth, E., Wirz-Justice, A., Alteration of internal circadian phase relationships after morning versus evening carbohydrate-rich meals in humans. J. Biol. Rhythms 17 (2002), 364–376.
24. Mistlberger, R.E., Skene, D.J., Nonphotic entrainment in humans?. J. Biol. Rhythms 20 (2005), 339–352.
25. Lamia, K.A., Storch, K.F., Weitz, C.J., Physiological significance of a peripheral tissue circadian clock. Proc. Natl. Acad. Sci. USA 105 (2008), 15172–15177.
26. Sadacca, L.A., Lamia, K.A., 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 (2011), 120–124.
27. Marcheva, B., Ramsey, K.M., Buhr, E.D., Kobayashi, Y., Su, H., Ko, C.H., Ivanova, G., Omura, C., Mo, S., Vitaterna, M.H., et al. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 466 (2010), 627–631.
28. Perelis, M., Marcheva, B., Ramsey, K.M., Schipma, M.J., Hutchison, A.L., Taguchi, A., Peek, C.B., Hong, H., Huang, W., Omura, C., et al. Pancreatic β cell enhancers regulate rhythmic transcription of genes controlling insulin secretion. Science, 350, 2015, aac4250.
29. Dyar, K.A., Ciciliot, S., Wright, L.E., Biensø, R.S., Tagliazucchi, G.M., Patel, V.R., Forcato, M., Paz, M.I., Gudiksen, A., Solagna, F., et al. Muscle insulin sensitivity and glucose metabolism are controlled by the intrinsic muscle clock. Mol. Metab. 3 (2013), 29–41.
30. Rakshit, K., Hsu, T.W., Matveyenko, A.V., Bmal1 is required for beta cell compensatory expansion, survival and metabolic adaptation to diet-induced obesity in mice. Diabetologia 59 (2016), 734–743.
31. Boivin, D.B., James, F.O., Wu, A., Cho-Park, P.F., Xiong, H., Sun, Z.S., Circadian clock genes oscillate in human peripheral blood mononuclear cells. Blood 102 (2003), 4143–4145.
32. Loboda, A., Kraft, W.K., Fine, B., Joseph, J., Nebozhyn, M., Zhang, C., He, Y., Yang, X., Wright, C., Morris, M., et al. Diurnal variation of the human adipose transcriptome and the link to metabolic disease. BMC Med. Genomics, 2, 2009, 7.
33. Arendt, J., Bojkowski, C., Folkard, S., Franey, C., Marks, V., Minors, D., Waterhouse, J., Wever, R.A., Wildgruber, C., Wright, J., Some effects of melatonin and the control of its secretion in humans. Ciba Found. Symp. 117 (1985), 266–283.
34. Lewy, A.J., Ahmed, S., Jackson, J.M., Sack, R.L., Melatonin shifts human circadian rhythms according to a phase-response curve. Chronobiol. Int. 9 (1992), 380–392.
35. Burgess, H.J., Revell, V.L., Eastman, C.I., A three pulse phase response curve to three milligrams of melatonin in humans. J. Physiol. 586 (2008), 639–647.
36. Burke, T.M., Markwald, R.R., McHill, A.W., Chinoy, E.D., Snider, J.A., Bessman, S.C., Jung, C.M., O'Neill, J.S., Wright, K.P. Jr., Effects of caffeine on the human circadian clock in vivo and in vitro. Sci. Transl. Med., 7, 2015, 305ra146.
37. Khalsa, S.B., Jewett, M.E., Cajochen, C., Czeisler, C.A., A phase response curve to single bright light pulses in human subjects. J. Physiol. 549 (2003), 945–952.
38. Cuesta, M., Cermakian, N., Boivin, D.B., Glucocorticoids entrain molecular clock components in human peripheral cells. FASEB J. 29 (2015), 1360–1370.
39. Salgado-Delgado, R., Angeles-Castellanos, M., Saderi, N., Buijs, R.M., Escobar, C., Food intake during the normal activity phase prevents obesity and circadian desynchrony in a rat model of night work. Endocrinology 151 (2010), 1019–1029.
40. Horne, J.A., Ostberg, O., A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int. J. Chronobiol. 4 (1976), 97–110.
41. Roenneberg, T., Wirz-Justice, A., Merrow, M., Life between clocks: daily temporal patterns of human chronotypes. J. Biol. Rhythms 18 (2003), 80–90.
42. Buysse, D.J., Reynolds, C.F. 3rd, Monk, T.H., Berman, S.R., Kupfer, D.J., The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 28 (1989), 193–213.
43. Beck, A.T., Beamesderfer, A., Assessment of depression: the depression inventory. Mod. Probl. Pharmacopsychiatry 7 (1974), 151–169.
44. Beck, A.T., Rial, W.Y., Rickels, K., Short form of depression inventory: cross-validation. Psychol. Rep. 34 (1974), 1184–1186.
45. Johns, M.W., A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep 14 (1991), 540–545.
46. Johns, M.W., Reliability and factor analysis of the Epworth Sleepiness Scale. Sleep 15 (1992), 376–381.
47. Wehrens, S.M., Hampton, S.M., Finn, R.E., Skene, D.J., Effect of total sleep deprivation on postprandial metabolic and insulin responses in shift workers and non-shift workers. J. Endocrinol. 206 (2010), 205–215.
48. Akerstedt, T., Gillberg, M., Subjective and objective sleepiness in the active individual. Int. J. Neurosci. 52 (1990), 29–37.
49. Horne, J.A., Baulk, S.D., Awareness of sleepiness when driving. Psychophysiology 41 (2004), 161–165.
50. Flint, A., Raben, A., Blundell, J.E., Astrup, A., Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. Int. J. Obes. Relat. Metab. Disord. 24 (2000), 38–48.
51. Fraser, S., Cowen, P., Franklin, M., Franey, C., Arendt, J., Direct radioimmunoassay for melatonin in plasma. Clin. Chem. 29 (1983), 396–397.
52. Riad-Fahmy, D., Read, G.F., Gaskell, S.J., Dyas, J., Hindawi, R., A simple, direct radioimmunoassay for plasma cortisol, featuring a 125I radioligand and a solid-phase separation technique. Clin. Chem. 25 (1979), 665–668.
53. Sletten, T.L., Revell, V.L., Middleton, B., Lederle, K.A., Skene, D.J., Age-related changes in acute and phase-advancing responses to monochromatic light. J. Biol. Rhythms 24 (2009), 73–84.