Modulation of circadian clocks by nutrients and food factors

Figures & data

Fig. 1. Circadian phase shift by stimuli in cultured mouse explants.

Notes: Cultured tissue explants from Per2::Luciferase knock-in mice¹⁸⁾ were monitored using bioluminescence. Adding 10 nM insulin to culture medium altered circadian phase in white adipose (A), but not in lung (B) tissue. Decreasing temperature from 37 to 34 °C for six hours delayed circadian phase (C), whereas 10 nM dexamethasone (glucocorticoid analog) advanced phase in lung (D). Arrows, timing of stimuli; arrowheads, peak timing.

Table 1. Nutrients and food factors that modulate circadian clocks.

Factor	Effect	Organism	Reference No.
Caffeine	Period extension	Neurospora	[63]
	Period extension	Chlamydomonas reinhardtii	[64]
	Phase delay	Mouse SCN slices	[58]
	Period extension	Drosophila	[62]
	Period extension	Human U2OS cells, Mouse NIH3T3 cells, Mouse liver slices, Mice	[59]
	Period extension, Phase shift	Mouse MEF cells, Mice	[60]
	Period extension, Phase delay of melatonin rhythm	Human U2OS cells, Humans	[61]
Cinnamic acid	Period shortening	Mouse differentiated neuronal cells, Mice	[69]
DHA, EPA	Enhancement of food entrainment	Mice	[55]
Forskolin	Phase shift	Rat-1 cells, Mouse fibroblasts	[72,73]
Harmine	Period extension	Mouse NIH3T3 cells	[66]
	Period extension	Mouse MEF cells, Mouse differentiated neuronal cells, Mouse SCN slices	[67]
Lithium	Period extension of locomotor rhythm	Rats	[85]
	Period extension of locomotor rhythm	Hamsters	[86]
	Period extension	Mouse fibroblasts, Mouse lung and SCN slices, Mice	[87]
Nobiletin	Enhancement of amplitude	Mouse immortalized fibroblasts, Mice	[84]
Ornithine	Phase advance of melatonin rhythm	Rats	[88]
	Phase advance	Mice	[56]
Palmitate	Period extension, Phase shift	Mouse fibroblasts, Mouse differentiated adipocytes	[68]
Resveratrol	Phase shift	Rat-1 cells	[57]
Theophylline	Period extension	Chlamydomonas reinhardtii	[64]
	Period extension	Trifolium repens L.	[89]
High-fat diet	Period extension	Mice	[43]
High-salt diet	Phase advance of peripheral clocks	Mice	[53]
Ketogenic diet	Phase advance of locomotor onset	Mice	[51]
Rapidly digested starch	Enhancement of food entrainment	Mice	[54]

Fig. 2. Resveratrol shifts circadian phase of cultured fibroblasts.

Notes: Rat-1 fibroblasts were transfected with Bmal1-luciferase reporter gene and then bioluminescence was monitored. Adding 100 μM resveratrol delayed circadian phase compared with vehicle (DMSO). Immediately decreased luminescence probably due to luciferase inhibition.⁹⁰⁾ Arrow, timing of stimuli; arrowheads, peak timing.

Fig. 3. Caffeine lengthens circadian period of human U2OS cells.

Notes: Bioluminescence emitted by U2OS cells derived from human osteosarcoma stably expressing hPER2::Luciferase reporter gene³⁸⁾ incubated with indicated concentrations of caffeine (A) was monitored for several days. Caffeine dose dependently lengthened circadian period (B).

Yoo S, Yamazaki S, Lowrey P, et al. PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci USA. 2004;101:5339–5346.10.1073/pnas.0308709101

 PubMed Web of Science ®Google Scholar

Feldman JF. Circadian periodicity a neurospora: alteration by inhibitors of cyclic AMP phosphodiesterase. Science. 1975;190:789–790.10.1126/science.173018

 PubMed Web of Science ®Google Scholar

Goodenough JE, Bruce VG. The effects of caffeine and theophylline on the phototactic rhythm of chlamydomonas reinhardii. Biological Bulletin. 1980;159:649–655.10.2307/1540830

 Web of Science ®Google Scholar

Ding JM, Buchanan GF, Tischkau SA, et al. A neuronal ryanodine receptor mediates light-induced phase delays of the circadian clock. Nature. 1998;394:381–384.

 PubMed Web of Science ®Google Scholar

Wu MN, Ho K, Crocker A, et al. The effects of caffeine on sleep in Drosophila require pka activity, but not the adenosine receptor. J Neurosci. 2009;29:11029–11037.10.1523/JNEUROSCI.1653-09.2009

 PubMed Web of Science ®Google Scholar

Oike H, Kobori M, Suzuki T, et al. Caffeine lengthens circadian rhythms in mice. Biochem Biophys Res Commun. 2011;410:654–658.10.1016/j.bbrc.2011.06.049

 PubMed Web of Science ®Google Scholar

Narishige S, Kuwahara M, Shinozaki A, et al. Effects of caffeine on circadian phase, amplitude and period evaluated in cells in vitro and peripheral organs in vivo in PER2::LUCIFERASE mice. Br J Pharmacol. 2014;171:5858–5869.10.1111/bph.2014.171.issue-24

 PubMed Web of Science ®Google Scholar

Burke TM, Markwald RR, McHill AW, et al. Effects of caffeine on the human circadian clock in vivo and in vitro. Sci Transl Med. 2015;7: 305ra146.

 Web of Science ®Google Scholar

Oishi K, Yamamoto S, Oike H, et al. Cinnamic acid shortens the period of the circadian clock in mice. Biochemistry and Biophysics Reports. Forthcoming.

 Google Scholar

Furutani A, Ikeda Y, Itokawa M, et al. Fish oil accelerates diet-induced entrainment of the mouse peripheral clock via GPR120. PLOS ONE. 2015;10:e0132472.10.1371/journal.pone.0132472

 PubMed Web of Science ®Google Scholar

Onishi Y, Oishi K, Kawano Y, et al. The harmala alkaloid harmine is a modulator of circadian Bmal1 transcription. Biosci Rep. 2012;32:45–52.10.1042/BSR20110002

 PubMed Web of Science ®Google Scholar

Kondoh D, Yamamoto S, Tomita T, et al. Harmine lengthens circadian period of the mammalian molecular clock in the suprachiasmatic nucleus. Biol Pharm Bull. 2014;37:1422–1427.10.1248/bpb.b14-00229

 PubMed Web of Science ®Google Scholar

Engelmann W. Slowing down of circadian-rhythms by lithium ions. Z Naturforsch C J Biosci C. 1973;28:733–736.

 Web of Science ®Google Scholar

Hofmann K, Gunderothpalmowski M, Wiedenmann G, et al. Further evidence for period lengthening effect of Li+ on circadian-rhythms. Z Naturforsch C J Biosci C. 1978;33:231–234.

 PubMed Web of Science ®Google Scholar

Li J, Lu WQ, Beesley S, et al. Lithium impacts on the amplitude and period of the molecular circadian clockwork. PLoS ONE. 2012;7:e33292.10.1371/journal.pone.0033292

 PubMed Web of Science ®Google Scholar

He B, Nohara K, Park N, et al. The small molecule nobiletin targets the molecular oscillator to enhance circadian rhythms and protect against metabolic syndrome. Cell Metab. 2016;23:610–621.10.1016/j.cmet.2016.03.007

 PubMed Web of Science ®Google Scholar

Matsuo H, Iwamoto A, Otsuka T, et al. Effects of time of L-ornithine administration on the diurnal rhythms of plasma growth hormone, melatonin, and corticosterone levels in mice. Chronobiol Int. 2015;32:225–234.10.3109/07420528.2014.965312

 PubMed Web of Science ®Google Scholar

Fukuda T, Haraguchi A, Kuwahara M, et al. l-Ornithine affects peripheral clock gene expression in mice. Sci Rep. 2016;6:34665.10.1038/srep34665

 PubMed Web of Science ®Google Scholar

Kim SM, Neuendorff N, Chapkin RS, et al. Role of inflammatory signaling in the differential effects of saturated and poly-unsaturated fatty acids on peripheral circadian clocks. EBioMedicine. 2016;7:100–111.10.1016/j.ebiom.2016.03.037

 PubMed Web of Science ®Google Scholar

Oike H, Kobori M. Resveratrol regulates circadian clock genes in rat-1 fibroblast cells. Biosci Biotechnol Biochem. 2008;72:3038–3040.10.1271/bbb.80426

 PubMed Web of Science ®Google Scholar

Bollig I, Mayer K, Mayer WE, et al. Effects of cAMP, theophylline, imidazole, and 4-(3,4-dimethoxybenzyl)-2-imidazolidone on the leaf movement rhythm of Trifolium repens-a test of the cAMP-hypothesis of circadian rhythms. Planta. 1978;141:225–230.10.1007/BF00387893

 PubMed Web of Science ®Google Scholar

Kohsaka A, Laposky AD, Ramsey KM, et al. High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab. 2007;6:414–421.10.1016/j.cmet.2007.09.006

 PubMed Web of Science ®Google Scholar

Oike H, Nagai K, Fukushima T, et al. High-salt diet advances molecular circadian rhythms in mouse peripheral tissues. Biochem Biophys Res Commun. 2010;402:7–13.10.1016/j.bbrc.2010.09.072

 PubMed Web of Science ®Google Scholar

Oishi K, Uchida D, Ohkura N, et al. Ketogenic diet disrupts the circadian clock and increases hypofibrinolytic risk by inducing expression of plasminogen activator inhibitor-1. Arterioscler Thromb Vasc Biol. 2009;29:1571–1577.10.1161/ATVBAHA.109.190140

 PubMed Web of Science ®Google Scholar

Itokawa M, Hirao A, Nagahama H, et al. Time-restricted feeding of rapidly digested starches causes stronger entrainment of the liver clock in PER2::LUCIFERASE knock-in mice. Nutr Res. 2013;33:109–119.10.1016/j.nutres.2012.12.004

 PubMed Web of Science ®Google Scholar

Bakhtiarova A, Taslimi P, Elliman SJ, et al. Resveratrol inhibits firefly luciferase. Biochem Biophys Res Commun. 2006;351:481–484.10.1016/j.bbrc.2006.10.057

 PubMed Web of Science ®Google Scholar

Isojima Y, Nakajima M, Ukai H, et al. CKIε/δ-dependent phosphorylation is a temperature-insensitive, period-determining process in the mammalian circadian clock. Proc Natl Acad Sci USA. 2009;106:15744–15749.10.1073/pnas.0908733106

 PubMed Web of Science ®Google Scholar