Insulin/IGF-1 Drives PERIOD Synthesis to Entrain Circadian Rhythms with Feeding Time
Open accessAbstract
In mammals, endogenous circadian clocks sense and respond to daily feeding and lighting cues, adjusting internal ∼24 h rhythms to resonate with, and anticipate, external cycles of day and night. The mechanism underlying circadian entrainment to feeding time is critical for understanding why mistimed feeding, as occurs during shift work, disrupts circadian physiology, a state that is associated with increased incidence of chronic diseases such as type 2 (T2) diabetes. We show that feeding-regulated hormones insulin and insulin-like growth factor 1 (IGF-1) reset circadian clocks in vivo and in vitro by induction of PERIOD proteins, and mistimed insulin signaling disrupts circadian organization of mouse behavior and clock gene expression. Insulin and IGF-1 receptor signaling is sufficient to determine essential circadian parameters, principally via increased PERIOD protein synthesis. This requires coincident mechanistic target of rapamycin (mTOR) activation, increased phosphoinositide signaling, and microRNA downregulation. Besides its well-known homeostatic functions, we propose insulin and IGF-1 are primary signals of feeding time to cellular clocks throughout the body.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche
Sato, T., Vries, R. G., Snippert, H. J., van de Wetering, M., Barker, N., Stange, D. E., van Es, J. H., Abo, A., Kujala, P., Peters, P. J., et al. (2009) · Nature · doi:10.1038/nature07935 · Cited by 7,204 · see citing works
Self-citationPhototransduction by retinal ganglion cells that set the circadian clock
Berson, D. M., Dunn, F. A., & Takao, M. (2002) · Science · doi:10.1126/science.1067262 · Cited by 3,629 · see citing works
Molecular Bases for Circadian Clocks
Dunlap, J. C. (1999) · Cell · doi:10.1016/s0092-8674(00)80566-8 · Cited by 2,900 · see citing works
Transcriptional architecture of the mammalian circadian clock
Takahashi, J. S. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.150 · Cited by 2,639 · see citing works
Damiola, F., Le Minh, N., Preitner, N., Kornmann, B., Fleury-Olela, F., & Schibler, U. (2000) · Genes & Development · doi:10.1101/gad.183500 · Cited by 2,394 · see citing works
Adverse metabolic and cardiovascular consequences of circadian misalignment
Scheer, F. A. J. L., Hilton, M. F., Mantzoros, C. S., & Shea, S. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808180106 · Cited by 2,351 · see citing works
Yoo, S.-H., Yamazaki, S., Lowrey, P. L., Shimomura, K., Ko, C. H., Buhr, E. D., Siepka, S. M., Hong, H.-K., Oh, W. J., Yoo, O. J., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308709101 · Cited by 2,329 · see citing works
Resetting of circadian time in peripheral tissues by glucocorticoid signaling
Balsalobre, A., Brown, S. A., Marcacci, L., Tronche, F., Kellendonk, C., Reichardt, H. M., Schütz, G., & Schibler, U. (2000) · Science · doi:10.1126/science.289.5488.2344 · Cited by 1,859 · see citing works
miRDB: an online resource for microRNA target prediction and functional annotations
Wong, N. W., & Wang, X. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku1104 · Cited by 1,762 · see citing works
Suprachiasmatic Nucleus: Cell Autonomy and Network Properties
Welsh, D. K., Takahashi, J. S., & Kay, S. A. (2010) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021909-135919 · Cited by 1,216 · see citing works
Making new contacts: the mTOR network in metabolism and signalling crosstalk
Shimobayashi, M., & Hall, M. N. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3757 · Cited by 1,053 · see citing works
Synchronization of Cellular Clocks in the Suprachiasmatic Nucleus
Yamaguchi, S., Isejima, H., Matsuo, T., Okura, R., Yagita, K., Kobayashi, M., & Okamura, H. (2003) · Science · doi:10.1126/science.1089287 · Cited by 934 · see citing works
Green, C. B., Takahashi, J. S., & Bass, J. (2008) · Cell · doi:10.1016/j.cell.2008.08.022 · Cited by 902 · cited 1× · see citing works
“Circadian rhythms, endogenous 24 h oscillations, are intrinsic to the biology of most multicellular organisms (Dunlap, 1999; Roenneberg andMerrow, 2005), controlling the temporal organization of many physiological and cellular functions (Green et al., 2008).”
Signal integration by mTORC1 coordinates nutrient input with biosynthetic output
Dibble, C. C., & Manning, B. D. (2013) · Nature Cell Biology · doi:10.1038/ncb2763 · Cited by 716 · see citing works
Circadian topology of metabolism
Bass, J. T. (2012) · Nature · doi:10.1038/nature11704 · Cited by 610 · see citing works
Cryptochromes mediate rhythmic repression of the glucocorticoid receptor
Lamia, K. A., Papp, S. J., Yu, R. T., Barish, G. D., Uhlenhaut, N. H., Jonker, J. W., Downes, M., & Evans, R. M. (2011) · Nature · doi:10.1038/nature10700 · Cited by 590 · see citing works
Multiple signaling pathways elicit circadian gene expression in cultured Rat-1 fibroblasts
Balsalobre, A., Marcacci, L., & Schibler, U. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00758-2 · Cited by 485 · see citing works
Buijs, R. M., Wortel, J., Van Heerikhuize, J. J., Feenstra, M. G. P., Ter Horst, G. J., Romijn, H. J., & Kalsbeek, A. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00575.x · Cited by 485 · see citing works
Glucocorticoid hormones inhibit food‐induced phase‐shifting of peripheral circadian oscillators
Minh, N. L., Damiola, F., Tronche, F., Schütz, G., & Schibler, U. (2001) · The EMBO Journal · doi:10.1093/emboj/20.24.7128 · Cited by 467 · see citing works
Signalling by insulin and IGF receptors: supporting acts and new players
Siddle, K. (2011) · Journal of Molecular Endocrinology · doi:10.1530/jme-11-0022 · Cited by 456 · see citing works
Photoentrainment and pupillary light reflex are mediated by distinct populations of ipRGCs
Chen, S., Badea, T. C., & Hattar, S. S. (2011) · Nature · doi:10.1038/nature10206 · Cited by 436 · see citing works
A Genome-wide RNAi Screen for Modifiers of the Circadian Clock in Human Cells
Zhang, E. E., Liu, A. C., Hirota, T., Miraglia, L. J., Welch, G. L., Pongsawakul, P. Y., Liu, X., Atwood, A., Huss, J. W., Janes, J. O., et al. (2009) · Cell · doi:10.1016/j.cell.2009.08.031 · Cited by 432 · see citing works
Glucocorticoid regulation of the circadian clock modulates glucose homeostasis
So, A. Y.-L., Bernal, T. U., Pillsbury, M. L., Yamamoto, K. R., & Feldman, B. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909733106 · Cited by 431 · cited 1× · see citing works
“, 2015), primarily by increasing Per gene transcription (So et al., 2009; Yurtsever et al., 2016).”
Constant light desynchronizes mammalian clock neurons
Ohta, H., Yamazaki, S., & McMahon, D. G. (2005) · Nature Neuroscience · doi:10.1038/nn1395 · Cited by 405 · see citing works
Mistimed sleep disrupts circadian regulation of the human transcriptome
Archer, S. N., Laing, E. E., Möller-Levet, C. S., van der Veen, D. R., Bucca, G., Lazar, A. S., Santhi, N., Slak, A., Kabiljo, R., von Schantz, M., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1316335111 · Cited by 386 · see citing works
Strengths and Limitations of Period Estimation Methods for Circadian Data
Zieliński, T., Moore, A., Troup, E., Halliday, K., & Millar, A. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0096462 · Cited by 344 · see citing works
The Circadian Protein BMAL1 Regulates Translation in Response to S6K1-Mediated Phosphorylation
Lipton, J. O., Yuan, E. D., Boyle, L. M., Ebrahimi‐Fakhari, D., Kwiatkowski, E. R., Nathan, A., Guettler, T., Davis, F. C., Asara, J. M., & Şahin, M. (2015) · Cell · doi:10.1016/j.cell.2015.04.002 · Cited by 342 · see citing works
Mauvoisin, D., Wang, J., Jouffe, C., Martin, E., Atger, F., Waridel, P., Quadroni, M., Gachon, F., & Naef, F. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1314066111 · Cited by 329 · see citing works
Signaling by insulin-like growth factor 1 in brain
Bondy, C. A., & Cheng, C. M. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2004.02.042 · Cited by 323 · see citing works
Hirota, T., Okano, T., Kokame, K., Shirotani-Ikejima, H., Miyata, T., & Fukada, Y. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m206233200 · Cited by 317 · see citing works
Clock-Talk: Interactions between Central and Peripheral Circadian Oscillators in MammalsPreprint
Schibler, U., Gotić, I., Saini, C., Gos, P., Curie, T., Emmenegger, Y., Sinturel, F., Gosselin, P., Gerber, A., Fleury-Olela, F., et al. (2015) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2015.80.027490 · Cited by 313 · see citing works
NS21: Re-defined and modified supplement B27 for neuronal cultures
Chen, Y., Stevens, B., Chang, J., Milbrandt, J., Barres, B. A., & Hell, J. W. (2008) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2008.03.013 · Cited by 301 · see citing works
Establishing Primary Adult Fibroblast Cultures From Rodents
Seluanov, A., Vaidya, A. M., & Gorbunova, V. A. (2010) · Journal of Visualized Experiments · doi:10.3791/2033 · Cited by 299 · see citing works
Analysis of Gene Regulatory Networks in the Mammalian Circadian Rhythm
Yan, J., Wang, H., Liu, Y., & Shao, C. (2008) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000193 · Cited by 297 · see citing works
Maywood, E. S., Chesham, J. E., O’Brien, J., & Hastings, M. H. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1101767108 · Cited by 284 · see citing works
Self-citationBMS-754807, a small molecule inhibitor of insulin-like growth factor-1R/IR
Carboni, J. M., Wittman, M. D., Yang, Z., Lee, F. Y., Greer, A. L., Hurlburt, W. W., Hillerman, S. M., Cao, C., Cantor, G. H., Dell-John, J., et al. (2009) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-09-0499 · Cited by 278 · see citing works
Assay of protein kinases using radiolabeled ATP: a protocol
Hastie, C. J., McLauchlan, H., & Cohen, P. (2006) · Nature Protocols · doi:10.1038/nprot.2006.149 · Cited by 253 · see citing works
Entrainment of disrupted circadian behavior through inhibition of casein kinase 1 (CK1) enzymes
Meng, Q., Maywood, E. S., Bechtold, D. A., Lu, W., Li, J., Gibbs, J. E., Dupré, S. M., Chesham, J. E., Rajamohan, F., Knafels, J. D., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005101107 · Cited by 253 · see citing works
Self-citationInsights into insulin resistance and type 2 diabetes from knockout mouse models
Kadowaki, T. (2000) · Journal of Clinical Investigation · doi:10.1172/jci10830 · Cited by 252 · see citing works
Ye, R., Selby, C. P., Chiou, Y., Ozkan‐Dagliyan, I., Gaddameedhi, S., & Sancar, A. (2014) · Genes & Development · doi:10.1101/gad.249417.114 · Cited by 247 · see citing works
Macromolecular Assemblies of the Mammalian Circadian Clock
Aryal, R. P., Kwak, P. B., Tamayo, A. G., Gebert, M., Chiu, P., Walz, T., & Weitz, C. J. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.07.017 · Cited by 246 · see citing works
Chen, R., Schirmer, A. E., Lee, Y., Lee, H.-M., Kumar, V., Yoo, S. H., Takahashi, J. S., & Lee, C. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.10.012 · Cited by 225 · see citing works
Food-anticipatory circadian rhythms: concepts and methods
Mistlberger, R. E. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06965.x · Cited by 224 · see citing works
Daily rhythms of food-anticipatory behavioral activity do not require the known circadian clock
Storch, K.-F., & Weitz, C. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902063106 · Cited by 222 · see citing works
Circadian clocks — the fall and rise of physiology
Roenneberg, T., & Merrow, M. W. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1766 · Cited by 203 · see citing works
Polysome Fractionation and Analysis of Mammalian Translatomes on a Genome-wide Scale
Gandin, V., Sikström, K., Alain, T., Morita, M., McLaughlan, S., Larsson, O. S., & Topisirović, I. (2014) · Journal of Visualized Experiments · doi:10.3791/51455 · Cited by 200 · see citing works
Slaaby, R., Schäffer, L., Lautrup-Larsen, I., Andersen, A. S., Shaw, A. C., Mathiasen, I. S., & Brandt, J. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m605189200 · Cited by 198 · see citing works
Degradation dynamics of microRNAs revealed by a novel pulse-chase approachPreprint
Marzi, M. J., Ghini, F., Cerruti, B., de Pretis, S., Bonetti, P., Giacomelli, C., Gorski, M. M., Kress, T. R., Pelizzola, M., Müller, H., et al. (2016) · Genome Research · doi:10.1101/gr.198788.115 · Cited by 184 · see citing works
Healthy clocks, healthy body, healthy mind
Reddy, A. B., & O'Neill, J. S. (2009) · Trends in Cell Biology · doi:10.1016/j.tcb.2009.10.005 · Cited by 182 · see citing works
Self-citationMukherji, A., Kobiita, A., Damara, M., Misra, N., Méziane, H., Champy, M., & Chambon, P. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1519807112 · Cited by 179 · see citing works
Dijk, D.-J., Duffy, J. F., Silva, E. J., Shanahan, T. L., Boivin, D. B., & Czeisler, C. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030037 · Cited by 170 · see citing works
Leney, S. E., & Tavaré, J. M. (2009) · Journal of Endocrinology · doi:10.1677/joe-09-0037 · Cited by 162 · see citing works
Salgado‐Delgado, R., Saderi, N., Basualdo, M. D. C., Guerrero‐Vargas, N. N., Escobar, C., & Buijs, R. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060052 · Cited by 159 · see citing works
Saini, C., Liani, A., Curie, T., Gos, P., Kreppel, F., Emmenegger, Y., Bonacina, L., Wolf, J., Poget, Y.-A., Franken, P., et al. (2013) · Genes & Development · doi:10.1101/gad.221374.113 · Cited by 154 · see citing works
Taniguchi, C. M., Tran, T. T., Kondo, T., Luo, J., Ueki, K., Cantley, L. C., & Kahn, C. R. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604628103 · Cited by 152 · see citing works
Granjon, A., Gustin, M., Rieusset, J., Lefai, É., Meugnier, E., Güller, I., Cerutti, C., Paultre, C. Z., Disse, E., RABASA-LHORET, R. P. R., et al. (2009) · Diabetes · doi:10.2337/db09-0165 · Cited by 142 · see citing works
Anticipation and entrainment to feeding time in intact and SCN-ablated C57BL/6j mice
Marchant, E. G., & Mistlberger, R. E. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00571-4 · Cited by 130 · see citing works
Mukherji, A., Kobiita, A., & Chambon, P. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1519735112 · Cited by 129 · see citing works
Environmental 24-hr Cycles Are Essential for Health
Lucassen, E. A., Coomans, C. P., van Putten, M., de Kreij, S. R., van Genugten, J. H. L. T., Sutorius, R. P. M., de Rooij, K. E., van der Velde, M., Verhoeve, S. L., Smit, J. W. A., et al. (2016) · Current Biology · doi:10.1016/j.cub.2016.05.038 · Cited by 129 · see citing works
miRNAs Are Required for Generating a Time Delay Critical for the Circadian Oscillator
Chen, R., D'Alessandro, M. R., & Lee, C. (2013) · Current Biology · doi:10.1016/j.cub.2013.08.005 · Cited by 127 · see citing works
Tahara, Y., Otsuka, M., Fuse, Y., Hirao, A., & Shibata, S. (2011) · Journal of Biological Rhythms · doi:10.1177/0748730411405958 · Cited by 125 · see citing works
Yamajuku, D., Inagaki, T., Haruma, T., Okubo, S., Kataoka, Y., Kobayashi, S., Ikegami, K., Laurent, T., Kojima, T., Noutomi, K., et al. (2012) · Scientific Reports · doi:10.1038/srep00439 · Cited by 123 · see citing works
Verhagen, L. A. W., Egecioglu, E., Luijendijk, M. C. M., Hillebrand, J. J., Adan, R. A. H., & Dickson, S. L. (2010) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2010.06.005 · Cited by 120 · see citing works
In vivo activation of insulin receptor tyrosine kinase by melatonin in the rat hypothalamus
Anhê, G. F., Caperuto, L. C., Pereira‐da‐Silva, M., Souza, L. C., Hirata, A. E., Velloso, L. A., Cipolla‐Neto, J., & Carvalho, C. R. D. O. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02514.x · Cited by 113 · see citing works
The Mysterious Food-Entrainable Oscillator: Insights from Mutant and Engineered Mouse Models
Pendergast, J. S., & Yamazaki, S. (2018) · Journal of Biological Rhythms · doi:10.1177/0748730418789043 · Cited by 110 · see citing works
Oxyntomodulin regulates resetting of the liver circadian clock by food
Landgraf, D., Tsang, A. H. K., Leliavski, A., Koch, C. E., Barclay, J. L., Drucker, D. J., & Oster, H. (2015) · eLife · doi:10.7554/elife.06253 · Cited by 103 · see citing works
The Role of the Endocrine System in Feeding-Induced Tissue-Specific Circadian Entrainment
Sato, M., Murakami, M., Node, K., Matsumura, R., & Akashi, M. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.06.015 · Cited by 102 · see citing works
Insulin-like growth factor-I (IGF-I) and clinical nutrition
Livingstone, C. (2013) · Clinical Science · doi:10.1042/cs20120663 · Cited by 94 · see citing works
Welsh, D. K., Imaizumi, T., & Kay, S. A. (2005) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(05)93011-5 · Cited by 93 · see citing works
Glucose, but not fat, phase shifts the feeding-entrained circadian clock
Stephan, F. K., & Davidson, A. J. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00166-8 · Cited by 93 · see citing works
Deng, Z., Lei, X., Zhang, X., Zhang, H., Liu, S., Chen, Q., Hu, H., Wang, X., Ning, L., Cao, Y., et al. (2015) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjv005 · Cited by 91 · see citing works
Feeding cycles entrain circadian rhythms of locomotor activity in CS mice but not in C57BL/6J mice
Abe, H., Kida, M., Tsuji, K., et al. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90146-7 · Cited by 84 · see citing works
Establishing Primary Adult Fibroblast Cultures From Rodents
Seluanov, A., Vaidya, A. M., & Gorbunova, V. A. (2010) · Journal of Visualized Experiments · doi:10.3791/2033-v · Cited by 80 · see citing works
Riede, S. J., van der Vinne, V., & Hut, R. A. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.130757 · Cited by 76 · see citing works
Hou, X., Huang, F., Macedo, L. F., Harrington, S. C., Reeves, K. A., Greer, A. L., Finckenstein, F. G., Brodie, A., Gottardis, M. M., Carboni, J. M., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-1080 · Cited by 72 · see citing works
Putker, M., Crosby, P., Feeney, K. A., Hoyle, N. P., Costa, A. S. H., Gaude, E., Frezza, C., & O'Neill, J. S. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2016.6911 · Cited by 68 · see citing works
Self-citationMaywood, E. S., Drynan, L. F., Chesham, J. E., Edwards, M. D., Dardente, H., Fustin, J., Hazlerigg, D. G., O'Neill, J. S., Codner, G. F., Smyllie, N. J., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220894110 · Cited by 64 · see citing works
Self-citationPeriod determination in the food-entrainable and methamphetamine-sensitive circadian oscillator(s)
Pendergast, J. S., Oda, G. A., Niswender, K. D., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1206213109 · Cited by 61 · see citing works
Yu, Y., Kastin, A. J., & Pan, W. (2006) · Endocrinology · doi:10.1210/en.2006-0020 · Cited by 60 · see citing works
Food-anticipatory activity and liver per1-luc activity in diabetic transgenic rats
Davidson, A. J., Stokkan, K., Yamazaki, S., & Menaker, M. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00680-7 · Cited by 59 · see citing works
Polysome Fractionation and Analysis of Mammalian Translatomes on a Genome-wide Scale
Gandin, V., Sikström, K., Alain, T., Morita, M., McLaughlan, S., Larsson, O. S., & Topisirović, I. (2014) · Journal of Visualized Experiments · doi:10.3791/51455-v · Cited by 57 · see citing works
Feeney, K. A., Putker, M., Brancaccio, M., & O'Neill, J. S. (2016) · Journal of Biological Rhythms · doi:10.1177/0748730416668898 · Cited by 56 · see citing works
Self-citationRev-erbα in the brain is essential for circadian food entrainment
Delezie, J., Dumont, S., Sandu, C., Reibel, S., Pévet, P., & Challet, É. (2016) · Scientific Reports · doi:10.1038/srep29386 · Cited by 54 · see citing works
Strong resetting of the mammalian clock by constant light followed by constant darkness
Chen, R., Seo, D.-O., Bell, E., von Gall, C., & Lee, C. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.2191-08.2008 · Cited by 53 · see citing works
Circadian Regulation of Food-Anticipatory Activity in Molecular Clock–Deficient Mice
Takasu, N. N., Kurosawa, G., Tokuda, I. T., Mochizuki, A., Todo, T., & Nakamura, W. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048892 · Cited by 52 · see citing works
A tunable artificial circadian clock in clock-defective mice
D'Alessandro, M. R., Beesley, S., Kim, J. K., Chen, R., Abich, E., Cheng, W. Y., Yi, P., Takahashi, J. S., & Lee, C. (2015) · Nature Communications · doi:10.1038/ncomms9587 · Cited by 52 · see citing works
Hastings, M. H., Reddy, A. B., McMahon, D. G., & Maywood, E. S. (2005) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(05)93030-9 · Cited by 49 · see citing works
Self-citationRobust circadian rhythms in organoid cultures from PERIOD2::LUCIFERASE mouse small intestine
Moore, S. R., Pruszka, J., Vallance, J. E., Aihara, E., Matsuura, T., Montrose, M. H., Shroyer, N. F., & Hong, C. I. (2014) · Disease Models & Mechanisms · doi:10.1242/dmm.014399 · Cited by 46 · see citing works
Metabolic consequences of timed feeding in mice
Shamsi, N. A., Salkeld, M. D., Rattanatray, L., Voultsios, A., Varcoe, T. J., Boden, M. J., & Kennaway, D. J. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.02.021 · Cited by 39 · see citing works
Transient, Light-Induced Rhythmicity in mPER-Deficient Mice
Bae, K., & Weaver, D. R. (2007) · Journal of Biological Rhythms · doi:10.1177/0748730406296718 · Cited by 21 · see citing works
The acute and temporary modulation ofPERIODgenes by hydrocortisone in healthy subjects
Yurtsever, T., Schilling, T. M., Kölsch, M., Turner, J. D., Meyer, J., Schächinger, H., & Schote, A. B. (2016) · Chronobiology International · doi:10.1080/07420528.2016.1211668 · Cited by 19 · see citing works
mPeriod2 Brdm1 and other single Period mutant mice have normal food anticipatory activity
Pendergast, J. S., Wendroth, R. H., Stenner, R. C., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-15332-6 · Cited by 19 · see citing works
Crosby, P., Hoyle, N. P., & O'Neill, J. S. (2017) · Journal of Visualized Experiments · doi:10.3791/56623 · Cited by 15 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Time-restricted eating for the prevention and management of metabolic diseases
Manoogian, E. N. C., Chow, L. S., Taub, P. R., Laferrère, B., & Panda, S. (2022) · Endocrine Reviews · doi:10.1210/endrev/bnab027 · Cited by 344 · see citing works
Insulin-Like Growth Factor 1 (IGF-1) Signaling in Glucose Metabolism in Colorectal Cancer
Kasprzak, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22126434 · Cited by 248 · see citing works
Daytime eating prevents internal circadian misalignment and glucose intolerance in night work
Chellappa, S. L., Qian, J., Vujovic, N., Morris, C. J., Nedeltcheva, A., Nguyen, H., Rahman, N., Heng, S. W., Kelly, L., Kerlin-Monteiro, K., et al. (2021) · Science Advances · doi:10.1126/sciadv.abg9910 · Cited by 135 · see citing works
Mammalian circadian systems: Organization and modern life challenges
Finger, A., & Kramer, A. (2021) · Acta Physiologica · doi:10.1111/apha.13548 · Cited by 117 · see citing works
Liu, X., Zhang, Z., Song, Y., Xie, H., & Dong, M. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1065263 · Cited by 102 · see citing works
Can Circadian Eating Pattern Adjustments Reduce Risk or Prevent Development of T2D?
Harris, C., & Czaja, K. (2023) · Nutrients · doi:10.3390/nu15071762 · Cited by 13 · see citing works
Dynamic modulation of glucose utilisation by glucocorticoid rhythms in health and disease
Zavala, E., Gil-Gómez, C. A., Wedgwood, K. C. A., Burgess, R., Tsaneva-Atanasova, K., & Herrera-Valdez, M. A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.02.27.968354 · Cited by 8 · see citing works
- Authors
- Crosby, P., Hamnett, R., Putker, M., Hoyle, N. P., Reed, M., Karam, C. J., Maywood, E. S., Stangherlin, A., Chesham, J. E., Hayter, E. A., Rosenbrier-Ribeiro, L., Newham, P., Clevers, H., Bechtold, D. A., & O’Neill, J. S.
- Affiliations
- MRC Laboratory of Molecular Biology (GB)
- University of Manchester (GB)
- AstraZeneca (United Kingdom) (GB)
- Hubrecht Institute for Developmental Biology and Stem Cell Research (NL)
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2019-05
- Volume
- 177
- Issue
- 4
- Pages
- 896-909.e20
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC6506277
- OpenAlex
- W2942493572
- Cited by
- 309
- References
- 94
- Citations by year
- 2026: 21 · 2025: 37 · 2024: 41 · 2023: 55 · 2022: 44 · 2021: 57 · 2020: 36 · 2019: 18
- FWCI
- 21.30
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Cell (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (publishedVersion, other-oa)
- KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (publishedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (submittedVersion, other-oa)
- Funders
- Dutch Cancer Foundation (KWF BUIT2014-6637)
- AstraZeneca/LMB Blue Skies Initiative
- BBSRC (BB/J017744/1)
- MRC (MR/N003101/1, MC_UP_1201/4)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Health Sciences › Medicine › Physiology › Dietary Effects on Health
- Keywords
- insulin, insulin-like growth factor I, PERIOD protein, circadian rhythm, meal timing, circadian entrainment, shift work, type 2 diabetes, mTOR signaling, phosphoinositide signaling, microRNA, clock gene expression, insulin receptor signaling
- MeSH terms
- Animals, Circadian Rhythm, Feeding Behavior, Female, Insulin, Insulin-Like Growth Factor I, Male, Mammals, Mice, Inbred C57BL, Signal Transduction, Receptor, IGF Type 1, Mice, Period Circadian Proteins, Circadian Clocks
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
