Advertisement

Abstract

Biological clocks are autonomous anticipatory oscillators that play a critical role in the organization and information processing from genome to whole organisms. Transformative advances into the clock system have opened insight into fundamental mechanisms through which clocks program energy transfer from sunlight into organic matter and potential energy, in addition to cell development and genotoxic stress response. The identification of clocks in nearly every single cell of the body raises questions as to how this gives rise to rhythmic physiology in multicellular organisms and how environmental signals entrain clocks to geophysical time. Here, we consider advances in understanding how regulatory networks emergent in clocks give rise to cell type–specific functions within tissues to affect homeostasis.

Get full access to this article

View all available purchase options and get full access to this article.

References and Notes

1
Konopka R. J. and Benzer S., Clock mutants of Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 68, 2112–2116 (1971). 10.1073/pnas.68.9.211210.1073/pnas.68.9.2112
2
Hardin P. E., Hall J. C., and Rosbash M., Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343, 536–540 (1990). 10.1038/343536a010.1038/343536a0
3
Partch C. L., Green C. B., and Takahashi J. S., Molecular architecture of the mammalian circadian clock. Trends Cell Biol. 24, 90–99 (2014). 10.1016/j.tcb.2013.07.00210.1016/j.tcb.2013.07.002
4
Yin L., Wu N., Curtin J. C., Qatanani M., Szwergold N. R., Reid R. A., Waitt G. M., Parks D. J., Pearce K. H., Wisely G. B., and Lazar M. A., Rev-erbα, a heme sensor that coordinates metabolic and circadian pathways. Science 318, 1786–1789 (2007). 10.1126/science.115017910.1126/science.1150179
5
Raghuram S., Stayrook K. R., Huang P., Rogers P. M., Nosie A. K., McClure D. B., Burris L. L., Khorasanizadeh S., Burris T. P., and Rastinejad F., Identification of heme as the ligand for the orphan nuclear receptors REV-ERBα and REV-ERBβ. Nat. Struct. Mol. Biol. 14, 1207–1213 (2007). 10.1038/nsmb134410.1038/nsmb1344
6
Kallen J. A., Schlaeppi J. M., Bitsch F., Geisse S., Geiser M., Delhon I., and Fournier B., X-ray structure of the hRORα LBD at 1.63 A: Structural and functional data that cholesterol or a cholesterol derivative is the natural ligand of RORα. Structure 10, 1697–1707 (2002). 10.1016/S0969-2126(02)00912-710.1016/S0969-2126(02)00912-7
7
McIntosh B. E., Hogenesch J. B., and Bradfield C. A., Mammalian Per-Arnt-Sim proteins in environmental adaptation. Annu. Rev. Physiol. 72, 625–645 (2010). 10.1146/annurev-physiol-021909-13592210.1146/annurev-physiol-021909-135922
8
Mehra A., Shi M., Baker C. L., Colot H. V., Loros J. J., and Dunlap J. C., A role for casein kinase 2 in the mechanism underlying circadian temperature compensation. Cell 137, 749–760 (2009). 10.1016/j.cell.2009.03.01910.1016/j.cell.2009.03.019
9
Hurley J. M., Loros J. J., and Dunlap J. C., Circadian oscillators: Around the transcription-translation feedback loop and on to output. Trends Biochem. Sci. 41, 834–846 (2016). 10.1016/j.tibs.2016.07.00910.1016/j.tibs.2016.07.009
10
Jones C. R., Huang A. L., Ptáček L. J., and Fu Y.-H., Genetic basis of human circadian rhythm disorders. Exp. Neurol. 243, 28–33 (2013). 10.1016/j.expneurol.2012.07.01210.1016/j.expneurol.2012.07.012
11
Balsalobre A., Damiola F., and Schibler U., A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93, 929–937 (1998). 10.1016/S0092-8674(00)81199-X10.1016/S0092-8674(00)81199-X
12
Menet J. S., Rodriguez J., Abruzzi K. C., and Rosbash M., Nascent-Seq reveals novel features of mouse circadian transcriptional regulation. eLife 1, e00011 (2012). 10.7554/eLife.0001110.7554/eLife.00011
13
Zaret K. S., Lerner J., and Iwafuchi-Doi M., Chromatin scanning by dynamic binding of pioneer factors. Mol. Cell 62, 665–667 (2016). 10.1016/j.molcel.2016.05.02410.1016/j.molcel.2016.05.024
14
Panda S., Antoch M. P., Miller B. H., Su A. I., Schook A. B., Straume M., Schultz P. G., Kay S. A., Takahashi J. S., and Hogenesch J. B., Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109, 307–320 (2002). 10.1016/S0092-8674(02)00722-510.1016/S0092-8674(02)00722-5
15
Storch K.-F., Lipan O., Leykin I., Viswanathan N., Davis F. C., Wong W. H., and Weitz C. J., Extensive and divergent circadian gene expression in liver and heart. Nature 417, 78–83 (2002). 10.1038/nature74410.1038/nature744
16
Fang B., Everett L. J., Jager J., Briggs E., Armour S. M., Feng D., Roy A., Gerhart-Hines Z., Sun Z., and Lazar M. A., Circadian enhancers coordinate multiple phases of rhythmic gene transcription in vivo. Cell 159, 1140–1152 (2014). 10.1016/j.cell.2014.10.02210.1016/j.cell.2014.10.022
17
Perelis M., Marcheva B., Moynihan Ramsey K., Schipma M. J., Hutchison A. L., Taguchi A., Peek C. B., Hong H., Huang W., Omura C., Allred A. L., Bradfield C. A., Dinner A. R., Barish G. D., and Bass J., Pancreatic β cell enhancers regulate rhythmic transcription of genes controlling insulin secretion. Science 350, aac4250 (2015). 10.1126/science.aac425010.1126/science.aac4250
18
Feng D., Liu T., Sun Z., Bugge A., Mullican S. E., Alenghat T., Liu X. S., and Lazar M. A., A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism. Science 331, 1315–1319 (2011). 10.1126/science.119812510.1126/science.1198125
19
Koike N., Yoo S. H., Huang H. C., Kumar V., Lee C., Kim T. K., and Takahashi J. S., Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 338, 349–354 (2012). 10.1126/science.122633910.1126/science.1226339
20
Lee C. S., Friedman J. R., Fulmer J. T., and Kaestner K. H., The initiation of liver development is dependent on Foxa transcription factors. Nature 435, 944–947 (2005). 10.1038/nature0364910.1038/nature03649
21
DiTacchio L., Le H. D., Vollmers C., Hatori M., Witcher M., Secombe J., and Panda S., Histone lysine demethylase JARID1a activates CLOCK-BMAL1 and influences the circadian clock. Science 333, 1881–1885 (2011). 10.1126/science.120602210.1126/science.1206022
22
Duong H. A. and Weitz C. J., Temporal orchestration of repressive chromatin modifiers by circadian clock Period complexes. Nat. Struct. Mol. Biol. 21, 126–132 (2014). 10.1038/nsmb.274610.1038/nsmb.2746
23
Zhang Y., Fang B., Emmett M. J., Damle M., Sun Z., Feng D., Armour S. M., Remsberg J. R., Jager J., Soccio R. E., Steger D. J., and Lazar M. A., Discrete functions of nuclear receptor Rev-erbα couple metabolism to the clock. Science 348, 1488–1492 (2015). 10.1126/science.aab302110.1126/science.aab3021
24
Lamia K. A., Papp S. J., Yu R. T., Barish G. D., Uhlenhaut N. H., Jonker J. W., Downes M., and Evans R. M., Cryptochromes mediate rhythmic repression of the glucocorticoid receptor. Nature 480, 552–556 (2011).22170608
25
Rey G., Cesbron F., Rougemont J., Reinke H., Brunner M., and Naef F., Genome-wide and phase-specific DNA-binding rhythms of BMAL1 control circadian output functions in mouse liver. PLOS Biol. 9, e1000595 (2011). 10.1371/journal.pbio.100059510.1371/journal.pbio.1000595
26
Asher G., Gatfield D., Stratmann M., Reinke H., Dibner C., Kreppel F., Mostoslavsky R., Alt F. W., and Schibler U., SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134, 317–328 (2008). 10.1016/j.cell.2008.06.05010.1016/j.cell.2008.06.050
27
Nakahata Y., Kaluzova M., Grimaldi B., Sahar S., Hirayama J., Chen D., Guarente L. P., and Sassone-Corsi P., The NAD+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell 134, 329–340 (2008). 10.1016/j.cell.2008.07.00210.1016/j.cell.2008.07.002
28
Nakahata Y., Sahar S., Astarita G., Kaluzova M., and Sassone-Corsi P., Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science 324, 654–657 (2009). 10.1126/science.117080310.1126/science.1170803
29
Ramsey K. M., Yoshino J., Brace C. S., Abrassart D., Kobayashi Y., Marcheva B., Hong H. K., Chong J. L., Buhr E. D., Lee C., Takahashi J. S., Imai S., and Bass J., Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science 324, 651–654 (2009). 10.1126/science.117164110.1126/science.1171641
30
Peek C. B., Affinati A. H., Ramsey K. M., Kuo H. Y., Yu W., Sena L. A., Ilkayeva O., Marcheva B., Kobayashi Y., Omura C., Levine D. C., Bacsik D. J., Gius D., Newgard C. B., Goetzman E., Chandel N. S., Denu J. M., Mrksich M., and Bass J., Circadian clock NAD+ cycle drives mitochondrial oxidative metabolism in mice. Science 342, 1243417 (2013). 10.1126/science.124341710.1126/science.1243417
31
Chang H.-C. and Guarente L., SIRT1 mediates central circadian control in the SCN by a mechanism that decays with aging. Cell 153, 1448–1460 (2013). 10.1016/j.cell.2013.05.02710.1016/j.cell.2013.05.027
32
Kojima S., Sher-Chen E. L., and Green C. B., Circadian control of mRNA polyadenylation dynamics regulates rhythmic protein expression. Genes Dev. 26, 2724–2736 (2012). 10.1101/gad.208306.11210.1101/gad.208306.112
33
Reddy A. B., Karp N. A., Maywood E. S., Sage E. A., Deery M., O’Neill J. S., Wong G. K., Chesham J., Odell M., Lilley K. S., Kyriacou C. P., and Hastings M. H., Circadian orchestration of the hepatic proteome. Curr. Biol. 16, 1107–1115 (2006). 10.1016/j.cub.2006.04.02610.1016/j.cub.2006.04.026
34
Edgar R. S., Green E. W., Zhao Y., van Ooijen G., Olmedo M., Qin X., Xu Y., Pan M., Valekunja U. K., Feeney K. A., Maywood E. S., Hastings M. H., Baliga N. S., Merrow M., Millar A. J., Johnson C. H., Kyriacou C. P., O’Neill J. S., and Reddy A. B., Peroxiredoxins are conserved markers of circadian rhythms. Nature 485, 459–464 (2012).22622569
35
Kil I. S., Ryu K. W., Lee S. K., Kim J. Y., Chu S. Y., Kim J. H., Park S., and Rhee S. G., Circadian oscillation of sulfiredoxin in the mitochondria. Mol. Cell 59, 651–663 (2015). 10.1016/j.molcel.2015.06.03110.1016/j.molcel.2015.06.031
36
Provencio I., Jiang G., De Grip W. J., Hayes W. P., and Rollag M. D., Melanopsin: An opsin in melanophores, brain, and eye. Proc. Natl. Acad. Sci. U.S.A. 95, 340–345 (1998). 10.1073/pnas.95.1.34010.1073/pnas.95.1.340
37
Hattar S., Lucas R. J., Mrosovsky N., Thompson S., Douglas R. H., Hankins M. W., Lem J., Biel M., Hofmann F., Foster R. G., and Yau K. W., Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424, 75–81 (2003). 10.1038/nature0176110.1038/nature01761
38
Jagannath A., Butler R., Godinho S. I., Couch Y., Brown L. A., Vasudevan S. R., Flanagan K. C., Anthony D., Churchill G. C., Wood M. J., Steiner G., Ebeling M., Hossbach M., Wettstein J. G., Duffield G. E., Gatti S., Hankins M. W., Foster R. G., and Peirson S. N., The CRTC1-SIK1 pathway regulates entrainment of the circadian clock. Cell 154, 1100–1111 (2013). 10.1016/j.cell.2013.08.00410.1016/j.cell.2013.08.004
39
Wang T. A., Yu Y. V., Govindaiah G., Ye X., Artinian L., Coleman T. P., Sweedler J. V., Cox C. L., and Gillette M. U., Circadian rhythm of redox state regulates excitability in suprachiasmatic nucleus neurons. Science 337, 839–842 (2012). 10.1126/science.122282610.1126/science.1222826
40
Saper C. B., Scammell T. E., and Lu J., Hypothalamic regulation of sleep and circadian rhythms. Nature 437, 1257–1263 (2005). 10.1038/nature0428410.1038/nature04284
41
Lin L., Faraco J., Li R., Kadotani H., Rogers W., Lin X., Qiu X., de Jong P. J., Nishino S., and Mignot E., The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell 98, 365–376 (1999). 10.1016/S0092-8674(00)81965-010.1016/S0092-8674(00)81965-0
42
Funato H., Tsai A. L., Willie J. T., Kisanuki Y., Williams S. C., Sakurai T., and Yanagisawa M., Enhanced orexin receptor-2 signaling prevents diet-induced obesity and improves leptin sensitivity. Cell Metab. 9, 64–76 (2009). 10.1016/j.cmet.2008.10.01010.1016/j.cmet.2008.10.010
43
Turek F. W., Joshu C., Kohsaka A., Lin E., Ivanova G., McDearmon E., Laposky A., Losee-Olson S., Easton A., Jensen D. R., Eckel R. H., Takahashi J. S., and Bass J., Obesity and metabolic syndrome in circadian Clock mutant mice. Science 308, 1043–1045 (2005). 10.1126/science.110875010.1126/science.1108750
44
Laposky A. D., Bass J., Kohsaka A., and Turek F. W., Sleep and circadian rhythms: Key components in the regulation of energy metabolism. FEBS Lett. 582, 142–151 (2008). 10.1016/j.febslet.2007.06.07910.1016/j.febslet.2007.06.079
45
He Y., Jones C. R., Fujiki N., Xu Y., Guo B., Holder J. L. Jr., Rossner M. J., Nishino S., and Fu Y. H., The transcriptional repressor DEC2 regulates sleep length in mammals. Science 325, 866–870 (2009). 10.1126/science.117444310.1126/science.1174443
46
Aran A., Einen M., Lin L., Plazzi G., Nishino S., and Mignot E., Clinical and therapeutic aspects of childhood narcolepsy-cataplexy: A retrospective study of 51 children. Sleep 33, 1457–1464 (2010).21102987
47
Liu A. C., Welsh D. K., Ko C. H., Tran H. G., Zhang E. E., Priest A. A., Buhr E. D., Singer O., Meeker K., Verma I. M., Doyle F. J. 3rd, Takahashi J. S., and Kay S. A., Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell 129, 605–616 (2007). 10.1016/j.cell.2007.02.04710.1016/j.cell.2007.02.047
48
Damiola F., Le Minh N., Preitner N., Kornmann B., Fleury-Olela F., and Schibler U., Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 14, 2950–2961 (2000). 10.1101/gad.18350010.1101/gad.183500
49
Stokkan K. A., Yamazaki S., Tei H., Sakaki Y., and Menaker M., Entrainment of the circadian clock in the liver by feeding. Science 291, 490–493 (2001). 10.1126/science.291.5503.49010.1126/science.291.5503.490
50
Kohsaka A., Laposky A. D., Ramsey K. M., Estrada C., Joshu C., Kobayashi Y., Turek F. W., and Bass J., High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab. 6, 414–421 (2007). 10.1016/j.cmet.2007.09.00610.1016/j.cmet.2007.09.006
51
Eckel-Mahan K. L., Patel V. R., de Mateo S., Orozco-Solis R., Ceglia N. J., Sahar S., Dilag-Penilla S. A., Dyar K. A., Baldi P., and Sassone-Corsi P., Reprogramming of the circadian clock by nutritional challenge. Cell 155, 1464–1478 (2013). 10.1016/j.cell.2013.11.03410.1016/j.cell.2013.11.034
52
Balsalobre A., Brown S. A., Marcacci L., Tronche F., Kellendonk C., Reichardt H. M., Schütz G., and Schibler U., Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289, 2344–2347 (2000). 10.1126/science.289.5488.234410.1126/science.289.5488.2344
53
Saini C., Morf J., Stratmann M., Gos P., and Schibler U., Simulated body temperature rhythms reveal the phase-shifting behavior and plasticity of mammalian circadian oscillators. Genes Dev. 26, 567–580 (2012). 10.1101/gad.183251.11110.1101/gad.183251.111
54
Buhr E. D., Yoo S.-H., and Takahashi J. S., Temperature as a universal resetting cue for mammalian circadian oscillators. Science 330, 379–385 (2010).20947768
55
Gotic I., Omidi S., Fleury-Olela F., Molina N., Naef F., and Schibler U., Temperature regulates splicing efficiency of the cold-inducible RNA-binding protein gene Cirbp. Genes Dev. 30, 2005–2017 (2016). 10.1101/gad.287094.11610.1101/gad.287094.116
56
Gerber A., Esnault C., Aubert G., Treisman R., Pralong F., and Schibler U., Blood-borne circadian signal stimulates daily oscillations in actin dynamics and SRF activity. Cell 152, 492–503 (2013). 10.1016/j.cell.2012.12.02710.1016/j.cell.2012.12.027
57
Papagiannakopoulos T., Bauer M. R., Davidson S. M., Heimann M., Subbaraj L., Bhutkar A., Bartlebaugh J., Vander Heiden M. G., and Jacks T., Circadian rhythm disruption promotes lung tumorigenesis. Cell Metab. 24, 324–331 (2016). 10.1016/j.cmet.2016.07.00110.1016/j.cmet.2016.07.001
58
Janich P., Pascual G., Merlos-Suárez A., Batlle E., Ripperger J., Albrecht U., Cheng H. Y., Obrietan K., Di Croce L., and Benitah S. A., The circadian molecular clock creates epidermal stem cell heterogeneity. Nature 480, 209–214 (2011). 10.1038/nature1064910.1038/nature10649
59
Puram R. V., Kowalczyk M. S., de Boer C. G., Schneider R. K., Miller P. G., McConkey M., Tothova Z., Tejero H., Heckl D., Järås M., Chen M. C., Li H., Tamayo A., Cowley G. S., Rozenblatt-Rosen O., Al-Shahrour F., Regev A., and Ebert B. L., Core circadian clock genes regulate leukemia stem cells in AML. Cell 165, 303–316 (2016). 10.1016/j.cell.2016.03.01510.1016/j.cell.2016.03.015
60
Ouyang Y., Andersson C. R., Kondo T., Golden S. S., and Johnson C. H., Resonating circadian clocks enhance fitness in cyanobacteria. Proc. Natl. Acad. Sci. U.S.A. 95, 8660–8664 (1998). 10.1073/pnas.95.15.866010.1073/pnas.95.15.8660
61
Buxton O. M., Cain S. W., O’Connor S. P., Porter J. H., Duffy J. F., Wang W., Czeisler C. A., and Shea S. A., Adverse metabolic consequences in humans of prolonged sleep restriction combined with circadian disruption. Sci. Transl. Med. 4, 129ra43 (2012). 10.1126/scitranslmed.300320010.1126/scitranslmed.3003200
62
McHill A. W., Melanson E. L., Higgins J., Connick E., Moehlman T. M., Stothard E. R., and Wright K. P. Jr., Impact of circadian misalignment on energy metabolism during simulated nightshift work. Proc. Natl. Acad. Sci. U.S.A. 111, 17302–17307 (2014). 10.1073/pnas.141202111110.1073/pnas.1412021111
63
Arble D. M., Bass J., Laposky A. D., Vitaterna M. H., and Turek F. W., Circadian timing of food intake contributes to weight gain. Obesity (Silver Spring) 17, 2100–2102 (2009). 10.1038/oby.2009.26410.1038/oby.2009.264
64
Hatori M., Vollmers C., Zarrinpar A., DiTacchio L., Bushong E. A., Gill S., Leblanc M., Chaix A., Joens M., Fitzpatrick J. A., Ellisman M. H., and Panda S., Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab. 15, 848–860 (2012). 10.1016/j.cmet.2012.04.01910.1016/j.cmet.2012.04.019
65
Jakubowicz D., Froy O., Wainstein J., and Boaz M., Meal timing and composition influence ghrelin levels, appetite scores and weight loss maintenance in overweight and obese adults. Steroids 77, 323–331 (2012). 10.1016/j.steroids.2011.12.00610.1016/j.steroids.2011.12.006
66
Roenneberg T., Allebrandt K. V., Merrow M., and Vetter C., Social jetlag and obesity. Curr. Biol. 22, 939–943 (2012). 10.1016/j.cub.2012.03.03810.1016/j.cub.2012.03.038
67
Schernhammer E. S., Laden F., Speizer F. E., Willett W. C., Hunter D. J., Kawachi I., and Colditz G. A., Rotating night shifts and risk of breast cancer in women participating in the nurses’ health study. J. Natl. Cancer Inst. 93, 1563–1568 (2001). 10.1093/jnci/93.20.156310.1093/jnci/93.20.1563
68
Pan A., Schernhammer E. S., Sun Q., and Hu F. B., Rotating night shift work and risk of type 2 diabetes: Two prospective cohort studies in women. PLOS Med. 8, e1001141 (2011). 10.1371/journal.pmed.100114110.1371/journal.pmed.1001141
69
Chang A.-M., Aeschbach D., Duffy J. F., and Czeisler C. A., Evening use of light-emitting eReaders negatively affects sleep, circadian timing, and next-morning alertness. Proc. Natl. Acad. Sci. U.S.A. 112, 1232–1237 (2015). 10.1073/pnas.141849011210.1073/pnas.1418490112
70
Nakamura T. J., Nakamura W., Yamazaki S., Kudo T., Cutler T., Colwell C. S., and Block G. D., Age-related decline in circadian output. J. Neurosci. 31, 10201–10205 (2011). 10.1523/JNEUROSCI.0451-11.201110.1523/JNEUROSCI.0451-11.2011
71
Katewa S. D., Akagi K., Bose N., Rakshit K., Camarella T., Zheng X., Hall D., Davis S., Nelson C. S., Brem R. B., Ramanathan A., Sehgal A., Giebultowicz J. M., and Kapahi P., Peripheral circadian clocks mediate dietary restriction-dependent changes in lifespan and fat metabolism in Drosophila. Cell Metab. 23, 143–154 (2016). 10.1016/j.cmet.2015.10.01410.1016/j.cmet.2015.10.014
72
Kondratov R. V., Kondratova A. A., Gorbacheva V. Y., Vykhovanets O. V., and Antoch M. P., Early aging and age-related pathologies in mice deficient in BMAL1, the core componentof the circadian clock. Genes Dev. 20, 1868–1873 (2006). 10.1101/gad.143220610.1101/gad.1432206
73
Fu L., Pelicano H., Liu J., Huang P., and Lee C., The circadian gene Period2 plays an important role in tumor suppression and DNA damage response in vivo. Cell 111, 41–50 (2002). 10.1016/S0092-8674(02)00961-310.1016/S0092-8674(02)00961-3
74
Ozturk N., Lee J. H., Gaddameedhi S., and Sancar A., Loss of cryptochrome reduces cancer risk in p53 mutant mice. Proc. Natl. Acad. Sci. U.S.A. 106, 2841–2846 (2009). 10.1073/pnas.081302810610.1073/pnas.0813028106
75
Papp S. J., Huber A. L., Jordan S. D., Kriebs A., Nguyen M., Moresco J. J., Yates J. R. III, and Lamia K. A., DNA damage shifts circadian clock time via Hausp-dependent Cry1 stabilization. eLife 4, e04883 (2015). 10.7554/eLife.0488310.7554/eLife.04883
76
Altman B. J., Hsieh A. L., Sengupta A., Krishnanaiah S. Y., Stine Z. E., Walton Z. E., Gouw A. M., Venkataraman A., Li B., Goraksha-Hicks P., Diskin S. J., Bellovin D. I., Simon M. C., Rathmell J. C., Lazar M. A., Maris J. M., Felsher D. W., Hogenesch J. B., Weljie A. M., and Dang C. V., MYC disrupts the circadian clock and metabolism in cancer cells. Cell Metab. 22, 1009–1019 (2015). 10.1016/j.cmet.2015.09.00310.1016/j.cmet.2015.09.003
77
Gaddameedhi S., Selby C. P., Kaufmann W. K., Smart R. C., and Sancar A., Control of skin cancer by the circadian rhythm. Proc. Natl. Acad. Sci. U.S.A. 108, 18790–18795 (2011). 10.1073/pnas.111524910810.1073/pnas.1115249108
78
Dulong S., Ballesta A., Okyar A., and Lévi F., Identification of circadian determinants of cancer chronotherapy through in vitro chronopharmacology and mathematical modeling. Mol. Cancer Ther. 14, 2154–2164 (2015). 10.1158/1535-7163.MCT-15-012910.1158/1535-7163.MCT-15-0129
79
Van Cauter E., Polonsky K. S., and Scheen A. J., Roles of circadian rhythmicity and sleep in human glucose regulation. Endocr. Rev. 18, 716–738 (1997).9331550
80
Dupuis J., Langenberg C., Prokopenko I., Saxena R., Soranzo N., Jackson A. U., Wheeler E., Glazer N. L., Bouatia-Naji N., Gloyn A. L., Lindgren C. M., Mägi R., Morris A. P., Randall J., Johnson T., Elliott P., Rybin D., Thorleifsson G., Steinthorsdottir V., Henneman P., Grallert H., Dehghan A., Hottenga J. J., Franklin C. S., Navarro P., Song K., Goel A., Perry J. R., Egan J. M., Lajunen T., Grarup N., Sparsø T., Doney A., Voight B. F., Stringham H. M., Li M., Kanoni S., Shrader P., Cavalcanti-Proença C., Kumari M., Qi L., Timpson N. J., Gieger C., Zabena C., Rocheleau G., Ingelsson E., An P., O’Connell J., Luan J., Elliott A., McCarroll S. A., Payne F., Roccasecca R. M., Pattou F., Sethupathy P., Ardlie K., Ariyurek Y., Balkau B., Barter P., Beilby J. P., Ben-Shlomo Y., Benediktsson R., Bennett A. J., Bergmann S., Bochud M., Boerwinkle E., Bonnefond A., Bonnycastle L. L., Borch-Johnsen K., Böttcher Y., Brunner E., Bumpstead S. J., Charpentier G., Chen Y. D., Chines P., Clarke R., Coin L. J., Cooper M. N., Cornelis M., Crawford G., Crisponi L., Day I. N., de Geus E. J., Delplanque J., Dina C., Erdos M. R., Fedson A. C., Fischer-Rosinsky A., Forouhi N. G., Fox C. S., Frants R., Franzosi M. G., Galan P., Goodarzi M. O., Graessler J., Groves C. J., Grundy S., Gwilliam R., Gyllensten U., Hadjadj S., Hallmans G., Hammond N., Han X., Hartikainen A. L., Hassanali N., Hayward C., Heath S. C., Hercberg S., Herder C., Hicks A. A., Hillman D. R., Hingorani A. D., Hofman A., Hui J., Hung J., Isomaa B., Johnson P. R., Jørgensen T., Jula A., Kaakinen M., Kaprio J., Kesaniemi Y. A., Kivimaki M., Knight B., Koskinen S., Kovacs P., Kyvik K. O., Lathrop G. M., Lawlor D. A., Le Bacquer O., Lecoeur C., Li Y., Lyssenko V., Mahley R., Mangino M., Manning A. K., Martínez-Larrad M. T., McAteer J. B., McCulloch L. J., McPherson R., Meisinger C., Melzer D., Meyre D., Mitchell B. D., Morken M. A., Mukherjee S., Naitza S., Narisu N., Neville M. J., Oostra B. A., Orrù M., Pakyz R., Palmer C. N., Paolisso G., Pattaro C., Pearson D., Peden J. F., Pedersen N. L., Perola M., Pfeiffer A. F., Pichler I., Polasek O., Posthuma D., Potter S. C., Pouta A., Province M. A., Psaty B. M., Rathmann W., Rayner N. W., Rice K., Ripatti S., Rivadeneira F., Roden M., Rolandsson O., Sandbaek A., Sandhu M., Sanna S., Sayer A. A., Scheet P., Scott L. J., Seedorf U., Sharp S. J., Shields B., Sigurethsson G., Sijbrands E. J., Silveira A., Simpson L., Singleton A., Smith N. L., Sovio U., Swift A., Syddall H., Syvänen A. C., Tanaka T., Thorand B., Tichet J., Tönjes A., Tuomi T., Uitterlinden A. G., van Dijk K. W., van Hoek M., Varma D., Visvikis-Siest S., Vitart V., Vogelzangs N., Waeber G., Wagner P. J., Walley A., Walters G. B., Ward K. L., Watkins H., Weedon M. N., Wild S. H., Willemsen G., Witteman J. C., Yarnell J. W., Zeggini E., Zelenika D., Zethelius B., Zhai G., Zhao J. H., Zillikens M. C., Borecki I. B., Loos R. J., Meneton P., Magnusson P. K., Nathan D. M., Williams G. H., Hattersley A. T., Silander K., Salomaa V., Smith G. D., Bornstein S. R., Schwarz P., Spranger J., Karpe F., Shuldiner A. R., Cooper C., Dedoussis G. V., Serrano-Ríos M., Morris A. D., Lind L., Palmer L. J., Hu F. B., Franks P. W., Ebrahim S., Marmot M., Kao W. H., Pankow J. S., Sampson M. J., Kuusisto J., Laakso M., Hansen T., Pedersen O., Pramstaller P. P., Wichmann H. E., Illig T., Rudan I., Wright A. F., Stumvoll M., Campbell H., Wilson J. F., Bergman R. N., Buchanan T. A., Collins F. S., Mohlke K. L., Tuomilehto J., Valle T. T., Altshuler D., Rotter J. I., Siscovick D. S., Penninx B. W., Boomsma D. I., Deloukas P., Spector T. D., Frayling T. M., Ferrucci L., Kong A., Thorsteinsdottir U., Stefansson K., van Duijn C. M., Aulchenko Y. S., Cao A., Scuteri A., Schlessinger D., Uda M., Ruokonen A., Jarvelin M. R., Waterworth D. M., Vollenweider P., Peltonen L., Mooser V., Abecasis G. R., Wareham N. J., Sladek R., Froguel P., Watanabe R. M., Meigs J. B., Groop L., Boehnke M., McCarthy M. I., Florez J. C., Barroso I., DIAGRAM Consortium, GIANT Consortium, Global BPgen Consortium, Anders Hamsten on behalf of Procardis Consortium, and MAGIC investigators, New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk. Nat. Genet. 42, 105–116 (2010). 10.1038/ng.52010.1038/ng.520
81
Bouatia-Naji N., Bonnefond A., Cavalcanti-Proença C., Sparsø T., Holmkvist J., Marchand M., Delplanque J., Lobbens S., Rocheleau G., Durand E., De Graeve F., Chèvre J. C., Borch-Johnsen K., Hartikainen A. L., Ruokonen A., Tichet J., Marre M., Weill J., Heude B., Tauber M., Lemaire K., Schuit F., Elliott P., Jørgensen T., Charpentier G., Hadjadj S., Cauchi S., Vaxillaire M., Sladek R., Visvikis-Siest S., Balkau B., Lévy-Marchal C., Pattou F., Meyre D., Blakemore A. I., Jarvelin M. R., Walley A. J., Hansen T., Dina C., Pedersen O., and Froguel P., A variant near MTNR1B is associated with increased fasting plasma glucose levels and type 2 diabetes risk. Nat. Genet. 41, 89–94 (2009). 10.1038/ng.27710.1038/ng.277
82
Marcheva B., Ramsey K. M., Buhr E. D., Kobayashi Y., Su H., Ko C. H., Ivanova G., Omura C., Mo S., Vitaterna M. H., Lopez J. P., Philipson L. H., Bradfield C. A., Crosby S. D., JeBailey L., Wang X., Takahashi J. S., and Bass J., Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 466, 627–631 (2010). 10.1038/nature0925310.1038/nature09253
83
Curtis A. M., Cheng Y., Kapoor S., Reilly D., Price T. S., and Fitzgerald G. A., Circadian variation of blood pressure and the vascular response to asynchronous stress. Proc. Natl. Acad. Sci. U.S.A. 104, 3450–3455 (2007). 10.1073/pnas.061168010410.1073/pnas.0611680104
84
Cheng B., Anea C. B., Yao L., Chen F., Patel V., Merloiu A., Pati P., Caldwell R. W., Fulton D. J., and Rudic R. D., Tissue-intrinsic dysfunction of circadian clock confers transplant arteriosclerosis. Proc. Natl. Acad. Sci. U.S.A. 108, 17147–17152 (2011). 10.1073/pnas.111299810810.1073/pnas.1112998108
85
Chen Z., Yoo S.-H., and Takahashi J. S., Small molecule modifiers of circadian clocks. Cell. Mol. Life Sci. 70, 2985–2998 (2013). 10.1007/s00018-012-1207-y10.1007/s00018-012-1207-y

(0)eLetters

eLetters is a forum for ongoing peer review. eLetters are not edited, proofread, or indexed, but they are screened. eLetters should provide substantive and scholarly commentary on the article. Embedded figures cannot be submitted, and we discourage the use of figures within eLetters in general. If a figure is essential, please include a link to the figure within the text of the eLetter. Please read our Terms of Service before submitting an eLetter.

Log In to Submit a Response

No eLetters have been published for this article yet.

Information & Authors

Information

Published In

Science
Volume 354 | Issue 6315
25 November 2016

Submission history

Published in print: 25 November 2016

Permissions

Request permissions for this article.

Acknowledgments

Work on circadian rhythms is supported in the J.B. laboratory by National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK) grants R01DK100814 and 2R01DK090625 and in the M.A.L. laboratory by NIDDK grant R01DK45586 and the JPB Foundation. M.A.L. serves on advisory boards for Pfizer and Eli Lilly and Company. J.B. has a financial interest in Reset Therapeutics, a biotechnology company developing therapeutics related to sleep and metabolism. We thank B. Marcheva for the figures. We apologize that space limitations prevented citation of all relevant literature.

Authors

Affiliations

Joseph Bass* [email protected]
Department of Medicine, Division of Endocrinology, Metabolism and Molecular Medicine, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA.
Mitchell A. Lazar* [email protected]
Division of Endocrinology, Diabetes, and Metabolism, Department of Medicine, Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
The Institute for Diabetes, Obesity, and Metabolism, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Notes

*
Corresponding author. Email: [email protected] (J.B.); [email protected] (M.A.L.)

Metrics & Citations

Metrics

Article Usage

Altmetrics

Citations

Cite as

Export citation

Select the format you want to export the citation of this publication.

Cited by

  1. Brain-muscle communication prevents muscle aging by maintaining daily physiology, Science, 384, 6695, (563-572), (2024)./doi/10.1126/science.adj8533
    Abstract
  2. Autonomous circadian rhythms in the human hepatocyte regulate hepatic drug metabolism and inflammatory responses, Science Advances, 10, 17, (2024)./doi/10.1126/sciadv.adm9281
    Abstract
  3. Circadian desynchrony and health, Atlas of Clinical Sleep Medicine, (168-174.e1), (2024).https://doi.org/10.1016/B978-0-323-65403-6.00029-9
    Crossref
  4. Role of Melatonin in Daily Variations of Plasma Insulin Level and Pancreatic Clock Gene Expression in Chick Exposed to Monochromatic Light, International Journal of Molecular Sciences, 24, 3, (2368), (2023).https://doi.org/10.3390/ijms24032368
    Crossref
  5. Circadian disruption does not alter tumorigenesis in a mouse model of lymphoma, F1000Research, 12, (49), (2023).https://doi.org/10.12688/f1000research.125272.1
    Crossref
  6. Brain nuclear receptors and cardiovascular function, Cell & Bioscience, 13, 1, (2023).https://doi.org/10.1186/s13578-023-00962-3
    Crossref
  7. Light at night and cause-specific mortality risk in Mainland China: a nationwide observational study, BMC Medicine, 21, 1, (2023).https://doi.org/10.1186/s12916-023-02822-w
    Crossref
  8. Chemotherapy delivery time affects treatment outcomes of female patients with diffuse large B cell lymphoma, JCI Insight, 8, 2, (2023).https://doi.org/10.1172/jci.insight.164767
    Crossref
  9. Circadian rhythm disruption in critically ill patients, Acta Physiologica, (2023).https://doi.org/10.1111/apha.13962
    Crossref
  10. When should I eat: A circadian view on food intake and metabolic regulation, Acta Physiologica, 237, 3, (2023).https://doi.org/10.1111/apha.13936
    Crossref
  11. See more
Loading...

View Options

Check Access

Log in to view the full text

AAAS ID LOGIN

AAAS login provides access to Science for AAAS Members, and access to other journals in the Science family to users who have purchased individual subscriptions.

Log in via OpenAthens.
Log in via Shibboleth.

More options

Register for free to read this article

As a service to the community, this article is available for free. Login or register for free to read this article.

Purchase this issue in print

Buy a single issue of Science for just $15 USD.

View options

PDF format

Download this article as a PDF file

Download PDF

Full Text

FULL TEXT

Media

Figures

Multimedia

Tables

Share

Share

Share article link

Share on social media