Circadian rhythms and proteomics: It's all about posttranslational modifications!

Focus Article

Daniel Mauvoisin

Published Online: Apr 29 2019

DOI: 10.1002/wsbm.1450

Full article on Wiley Online Library: HTML PDF

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Abstract The circadian clock is a molecular endogenous timekeeping system and allows organisms to adjust their physiology and behavior to the geophysical time. Organized hierarchically, the master clock in the suprachiasmatic nuclei, coordinates peripheral clocks, via direct, or indirect signals. In peripheral organs, such as the liver, the circadian clock coordinates gene expression, notably metabolic gene expression, from transcriptional to posttranslational level. The metabolism in return feeds back on the molecular circadian clock via posttranslational‐based mechanisms. During the last two decades, circadian gene expression studies have mostly been relying primarily on genomics or transcriptomics approaches and transcriptome analyses of multiple organs/tissues have revealed that the majority of protein‐coding genes display circadian rhythms in a tissue specific manner. More recently, new advances in mass spectrometry offered circadian proteomics new perspectives, that is, the possibilities of performing large scale proteomic studies at cellular and subcellular levels, but also at the posttranslational modification level. With important implications in metabolic health, cell signaling has been shown to be highly relevant to circadian rhythms. Moreover, comprehensive characterization studies of posttranslational modifications are emerging and as a result, cell signaling processes are expected to be more deeply characterized and understood in the coming years with the use of proteomics. This review summarizes the work studying diurnally rhythmic or circadian gene expression performed at the protein level. Based on the knowledge brought by circadian proteomics studies, this review will also discuss the role of posttranslational modification events as an important link between the molecular circadian clock and metabolic regulation. This article is categorized under: Laboratory Methods and Technologies > Proteomics Methods Physiology > Mammalian Physiology in Health and Disease Biological Mechanisms > Cell Signaling

Quantitative mass spectrometry approaches used in circadian/diurnal studies: Red and gray boxes or tubes represent the different experimental conditions and the stars indicate the steps at which samples are labeled and combined allowing the quantification of relative protein abundance in the different experimental conditions. Earlier labeling and samples combination decreases the risk of quantification errors due to technical experimental variations. **In the case of label free, the combination is performed post data acquisition by computational treatment of the mass spectrometry data

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Hierarchical organization of the mammalian molecular circadian clock. BMAL1, brain and muscle Arnt‐like protein‐1; CCGs, clockcontrolled genes; CLOCK, circadian locomotor output cycles kaput; CRY, Cryptochromes (CRY1, CRY2); Dbp, D site of albumin promoter (albumin D‐box) binding protein; PER, Periods (PER1, PER2); REV‐ERB's, REV‐ERBA alpha (NR1D1: nuclear receptor subfamily 1, group D, member 1), REV‐ERBA beta (NR1D2: nuclear receptor subfamily 1, group D, member 2); ROR, Retinoid‐related orphan receptors; SCN, suprachiasmatic nuclei; ZT, zeitgeber time

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Experimental design of the SILAC diurnal proteomic experiment in mouse liver used in Mauvoisin et al. (). SILAC, stable‐isotope labeling by amino acids in cell culture

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References

Allada,, R., Emery,, P., Takahashi,, J. S., & Rosbash,, M. (2001). Stopping time: The genetics of fly and mouse circadian clocks. Annual Review of Neuroscience, 24, 1091–1119.
Antoch,, M. P., Song,, E. J., Chang,, A. M., Vitaterna,, M. H., Zhao,, Y., Wilsbacher,, L. D., … Takahashi,, J. S. (1997). Functional identification of the mouse circadian clock gene by transgenic BAC rescue. Cell, 89(4), 655–667.
Aryal,, R. P., Kwak,, P. B., Tamayo,, A. G., Gebert,, M., Chiu,, P. L., Walz,, T., & Weitz,, C. J. (2017). Macromolecular assemblies of the mammalian circadian clock. Molecular Cell, 67(5), 770–782.
Asher,, G., Gatfield,, D., Stratmann,, M., Reinke,, H., Dibner,, C., Kreppel,, F., … Schibler,, U. (2008). SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell, 134(2), 317–328.
Asher,, G., Reinke,, H., Altmeyer,, M., Gutierrez‐Arcelus,, M., Hottiger,, M. O., & Schibler,, U. (2010). Poly(ADP‐ribose) polymerase 1 participates in the phase entrainment of circadian clocks to feeding. Cell, 142(6), 943–953.
Asher,, G., & Sassone‐Corsi,, P. (2015). Time for food: The intimate interplay between nutrition, metabolism, and the circadian clock. Cell, 161(1), 84–92.
Atger,, F., Gobet,, C., Marquis,, J., Martin,, E., Wang,, J., Weger,, B., … Gachon,, F. (2015). Circadian and feeding rhythms differentially affect rhythmic mRNA transcription and translation in mouse liver. Proceedings of the National Academy of Sciences of the United States of America, 112(47), E6579–E6588.
Atkins,, N., Jr., Mitchell,, J. W., Romanova,, E. V., Morgan,, D. J., Cominski,, T. P., Ecker,, J. L., … Gillette,, M. U. (2010). Circadian integration of glutamatergic signals by little SAAS in novel suprachiasmatic circuits. PLoS One, 5(9), e12612.
Baker,, C. L., Kettenbach,, A. N., Loros,, J. J., Gerber,, S. A., & Dunlap,, J. C. (2009). Quantitative proteomics reveals a dynamic interactome and phase‐specific phosphorylation in the Neurospora circadian clock. Molecular Cell, 34(3), 354–363.
Balsalobre,, A., Damiola,, F., & Schibler,, U. (1998). A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell, 93(6), 929–937.
Bantscheff,, M., Schirle,, M., Sweetman,, G., Rick,, J., & Kuster,, B. (2007). Quantitative mass spectrometry in proteomics: A critical review. Analytical and Bioanalytical Chemistry, 389(4), 1017–1031.
Bargiello,, T. A., Jackson,, F. R., & Young,, M. W. (1984). Restoration of circadian behavioural rhythms by gene transfer in Drosophila. Nature, 312(5996), 752–754.
Benegiamo,, G., Mure,, L. S., Erikson,, G., Le,, H. D., Moriggi,, E., Brown,, S. A., & Panda,, S. (2018). The RNA‐binding protein NONO coordinates hepatic adaptation to feeding. Cell Metabolism, 27, 404–418.
Berson,, D. M., Dunn,, F. A., & Takao,, M. (2002). Phototransduction by retinal ganglion cells that set the circadian clock. Science, 295(5557), 1070–1073.
Berthier,, A., Vinod,, M., Porez,, G., Steenackers,, A., Alexandre,, J., Yamakawa,, N., … Lefebvre,, P. (2018). Combinatorial regulation of hepatic cytoplasmic signaling and nuclear transcriptional events by the OGT/REV‐ERBalpha complex. Proceedings of the National Academy of Sciences of the United States of America, 115(47), E11033–E11042.
Brewer,, M., Lange,, D., Baler,, R., & Anzulovich,, A. (2005). SREBP‐1 as a transcriptional integrator of circadian and nutritional cues in the liver. Journal of Biological Rhythms, 20(3), 195–205.
Caratti,, G., Iqbal,, M., Hunter,, L., Kim,, D., Wang,, P., Vonslow,, R. M., … Ray,, D. W. (2018). REVERBa couples the circadian clock to hepatic glucocorticoid action. The Journal of Clinical Investigation, 128(10), 4454–4471.
Cardone,, L., Hirayama,, J., Giordano,, F., Tamaru,, T., Palvimo,, J. J., & Sassone‐Corsi,, P. (2005). Circadian clock control by SUMOylation of BMAL1. Science, 309(5739), 1390–1394.
Chaix,, A., Lin,, T., Le,, H. D., Chang,, M. W., & Panda,, S. (2019). Time‐restricted feeding prevents obesity and metabolic syndrome in mice lacking a circadian clock. Cell Metabolism, 29(2), 303–319.
Chaix,, A., Zarrinpar,, A., Miu,, P., & Panda,, S. (2014). Time‐restricted feeding is a preventative and therapeutic intervention against diverse nutritional challenges. Cell Metabolism, 20(6), 991–1005.
Chang,, H.‐C., & Guarente,, L. (2013). SIRT1 mediates central circadian control in the SCN by a mechanism that decays with aging. Cell, 153(7), 1448–1460.
Chao,, H. W., Doi,, M., Fustin,, J. M., Chen,, H., Murase,, K., Maeda,, Y., … Okamura,, H. (2017). Circadian clock regulates hepatic polyploidy by modulating Mkp1‐Erk1/2 signaling pathway. Nature Communications, 8(1), 2238.
Chawla,, A., & Lazar,, M. A. (1993). Induction of rev‐ErbA alpha, an orphan receptor encoded on the opposite strand of the alpha‐thyroid hormone receptor gene, during adipocyte differentiation. The Journal of Biological Chemistry, 268(22), 16265–16269.
Chiang,, C. K., Mehta,, N., Patel,, A., Zhang,, P., Ning,, Z., Mayne,, J., … Figeys,, D. (2014). The proteomic landscape of the suprachiasmatic nucleus clock reveals large‐scale coordination of key biological processes. PLoS Genetics, 10(10), e1004695.
Chiang,, C. K., Xu,, B., Mehta,, N., Mayne,, J., Sun,, W. Y., Cheng,, K., … Figeys,, D. (2017). Phosphoproteome profiling reveals circadian clock regulation of posttranslational modifications in the murine Hippocampus. Frontiers in Neurology, 8, 110.
Choudhary,, M. K., Nomura,, Y., Wang,, L., Nakagami,, H., & Somers,, D. E. (2015). Quantitative circadian phosphoproteomic analysis of Arabidopsis reveals extensive clock control of key components in physiological, metabolic, and signaling pathways. Molecular %26 Cellular Proteomics, 14(8), 2243–2260.
Cretenet,, G., Le Clech,, M., & Gachon,, F. (2010). Circadian clock‐coordinated 12 Hr period rhythmic activation of the IRE1alpha pathway controls lipid metabolism in mouse liver. Cell Metabolism, 11(1), 47–57.
Crowell,, A. M., Greene,, C. S., Loros,, J. J., & Dunlap,, J. C. (2018). Learning and imputation for mass‐spec Bias reduction (LIMBR). Bioinformatics, bty828.
Damiola,, F., Le Minh,, N., Preitner,, N., Kornmann,, B., Fleury‐Olela,, F., & Schibler,, U. (2000). Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes %26 Development, 14(23), 2950–2961.
Dang,, F., Sun,, X., Ma,, X., Wu,, R., Zhang,, D., Chen,, Y., … Liu,, Y. (2016). Insulin post‐transcriptionally modulates Bmal1 protein to affect the hepatic circadian clock. Nature Communications, 7, 12696.
de Goede,, P., Sen,, S., Su,, Y., Foppen,, E., Poirel,, V. J., Challet,, E., & Kalsbeek,, A. (2018). An Ultradian feeding schedule in rats affects metabolic gene expression in liver, Brown adipose tissue and skeletal muscle with only mild effects on circadian clocks. International Journal of Molecular Sciences, 19(10), 3171. https://doi.org/10.3390/ijms19103171
Deery,, M. J., Maywood,, E. S., Chesham,, J. E., Sládek,, M., Karp,, N. A., Green,, E. W., … Hastings,, M. H. (2009). Proteomic analysis reveals the role of synaptic vesicle cycling in sustaining the Suprachiasmatic circadian clock. Current Biology, 19(23), 2031–2036.
Dibner,, C., Schibler,, U., & Albrecht,, U. (2010). The mammalian circadian timing system: Organization and coordination of central and peripheral clocks. Annual Review of Physiology, 72, 517–549.
Diering,, G. H., Nirujogi,, R. S., Roth,, R. H., Worley,, P. F., Pandey,, A., & Huganir,, R. L. (2017). Homer1a drives homeostatic scaling‐down of excitatory synapses during sleep. Science, 355(6324), 511–515.
Du,, J., Zhang,, Y., Xue,, Y., Zhao,, X., Zhao,, X., Wei,, Y., … Zhao,, Z. (2018). Diurnal protein oscillation profiles in Drosophila head. FEBS Letters, 592, 3736–3749.
Du,, N. H., Arpat,, A. B., De Matos,, M., & Gatfield,, D. (2014). MicroRNAs shape circadian hepatic gene expression on a transcriptome‐wide scale. eLife, 3, e02510.
Edgar,, R. S., Green,, E. W., Zhao,, Y., van Ooijen,, G., Olmedo,, M., Qin,, X., … Reddy,, A. B. (2012). Peroxiredoxins are conserved markers of circadian rhythms. Nature, 485(7399), 459–464.
Edgar,, R. S., Stangherlin,, A., Nagy,, A. D., Nicoll,, M. P., Efstathiou,, S., O`Neill,, J. S., & Reddy,, A. B. (2016). Cell autonomous regulation of herpes and influenza virus infection by the circadian clock. Proceedings of the National Academy of Sciences of the United States of America, 113(36), 10085–10090.
Fahrenkrug,, J., Hannibal,, J., Honore,, B., & Vorum,, H. (2005). Altered calmodulin response to light in the suprachiasmatic nucleus of PAC1 receptor knockout mice revealed by proteomic analysis. Journal of Molecular Neuroscience, 25(3), 251–258.
Feng,, D., Liu,, T., Sun,, Z., Bugge,, A., Mullican,, S. E., Alenghat,, T., … Lazar,, M. A. (2011). A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism. Science, 331(6022), 1315–1319.
Gachon,, F. (2007). Physiological function of PARbZip circadian clock‐controlled transcription factors. Annals of Medicine, 39(8), 562–571.
Gachon,, F., Fonjallaz,, P., Damiola,, F., Gos,, P., Kodama,, T., Zakany,, J., … Schibler,, U. (2004). The loss of circadian PAR bZip transcription factors results in epilepsy. Genes %26 Development, 18(12), 1397–1412.
Gachon,, F., Olela,, F. F., Schaad,, O., Descombes,, P., & Schibler,, U. (2006). The circadian PAR‐domain basic leucine zipper transcription factors DBP, TEF, and HLF modulate basal and inducible xenobiotic detoxification. Cell Metabolism, 4(1), 25–36.
Gekakis,, N., Staknis,, D., Nguyen,, H. B., Davis,, F. C., Wilsbacher,, L. D., King,, D. P., … Weitz,, C. J. (1998). Role of the CLOCK protein in the mammalian circadian mechanism. Science, 280(5369), 1564–1569.
Gilardi,, F., Migliavacca,, E., Naldi,, A., Baruchet,, M., Canella,, D., Le Martelot,, G., … Desvergne,, B. (2014). Genome‐wide analysis of SREBP1 activity around the clock reveals its combined dependency on nutrient and circadian signals. PLoS Genetics, 10(3), e1004155.
Gobet,, C., & Naef,, F. (2017). Ribosome profiling and dynamic regulation of translation in mammals. Current Opinion in Genetics %26 Development, 43, 120–127.
Grimaldi,, B., Bellet,, M. M., Katada,, S., Astarita,, G., Hirayama,, J., Amin,, R. H., … Sassone‐Corsi,, P. (2010). PER2 controls lipid metabolism by direct regulation of PPARgamma. Cell Metabolism, 12(5), 509–520.
Hardin,, P. E., Hall,, J. C., & Rosbash,, M. (1990). Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature, 343(6258), 536–540.
Harmar,, A. J. (2003). An essential role for peptidergic signalling in the control of circadian rhythms in the suprachiasmatic nuclei. Journal of Neuroendocrinology, 15(4), 335–338.
Hatcher,, N. G., Atkins,, N., Jr., Annangudi,, S. P., Forbes,, A. J., Kelleher,, N. L., Gillette,, M. U., & Sweedler,, J. V. (2008). Mass spectrometry‐based discovery of circadian peptides. Proceedings of the National Academy of Sciences of the United States of America, 105(34), 12527–12532.
Hatori,, M., Vollmers,, C., Zarrinpar,, A., DiTacchio,, L., Bushong,, E. A., Gill,, S., … Panda,, S. (2012). Time‐restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high‐fat diet. Cell Metabolism, 15(6), 848–860.
Hattar,, S., Liao,, H. W., Takao,, M., Berson,, D. M., & Yau,, K. W. (2002). Melanopsin‐containing retinal ganglion cells: Architecture, projections, and intrinsic photosensitivity. Science, 295(5557), 1065–1070.
Hirano,, A., Braas,, D., Fu,, Y. H., & Ptacek,, L. J. (2017). FAD regulates CRYPTOCHROME protein stability and circadian clock in mice. Cell Reports, 19(2), 255–266.
Hirano,, A., Fu,, Y. H., & Ptacek,, L. J. (2016). The intricate dance of post‐translational modifications in the rhythm of life. Nature Structural %26 Molecular Biology, 23(12), 1053–1060.
Honma,, S., Ikeda,, M., Abe,, H., Tanahashi,, Y., Namihira,, M., Honma,, K., & Nomura,, M. (1998). Circadian oscillation of BMAL1, a partner of a mammalian clock gene clock, in rat suprachiasmatic nucleus. Biochemical and Biophysical Research Communications, 250(1), 83–87.
Honma,, S., Kawamoto,, T., Takagi,, Y., Fujimoto,, K., Sato,, F., Noshiro,, M., … Honma,, K. (2002). Dec1 and Dec2 are regulators of the mammalian molecular clock. Nature, 419(6909), 841–844.
Humphrey,, S. J., Azimifar,, S. B., & Mann,, M. (2015). High‐throughput phosphoproteomics reveals in vivo insulin signaling dynamics. Nature Biotechnology, 33(9), 990–995.
Hurley,, J. M., Jankowski,, M. S., De Los Santos,, H., Crowell,, A. M., Fordyce,, S. B., Zucker,, J. D., … Dunlap,, J. C. (2018). Circadian proteomic analysis uncovers mechanisms of post‐transcriptional regulation in metabolic pathways. Cell Systems, 7(6), 613–626.
Husse,, J., Leliavski,, A., Tsang,, A. H., Oster,, H., & Eichele,, G. (2014). The light‐dark cycle controls peripheral rhythmicity in mice with a genetically ablated suprachiasmatic nucleus clock. The FASEB Journal, 28(11), 4950–4960.
Itzhak,, D. N., Davies,, C., Tyanova,, S., Mishra,, A., Williamson,, J., Antrobus,, R., … Borner,, G. H. H. (2017). A mass spectrometry‐based approach for mapping protein subcellular localization reveals the spatial proteome of mouse primary neurons. Cell Reports, 20(11), 2706–2718.
Itzhak,, D. N., Schessner,, J. P., & Borner,, G. H. H. (2018). Dynamic Organellar Maps for Spatial Proteomics. Current Protocols in Cell Biology, e81. https://doi.org/10.1002/cpcb.81
Izumo,, M., Pejchal,, M., Schook,, A. C., Lange,, R. P., Walisser,, J. A., Sato,, T. R., … Takahashi,, J. S. (2014). Differential effects of light and feeding on circadian organization of peripheral clocks in a forebrain Bmal1 mutant. eLife, 3, e04617.
Jacobi,, D., Liu,, S., Burkewitz,, K., Kory,, N., Knudsen,, N. H., Alexander,, R. K., … Lee,, C. H. (2015). Hepatic Bmal1 regulates rhythmic mitochondrial dynamics and promotes metabolic fitness. Cell Metabolism, 22(4), 709–720.
Jang,, C., Lahens,, N. F., Hogenesch,, J. B., & Sehgal,, A. (2015). Ribosome profiling reveals an important role for translational control in circadian gene expression. Genome Research, 25(12), 1836–1847.
Janich,, P., Arpat,, A. B., Castelo‐Szekely,, V., Lopes,, M., & Gatfield,, D. (2015). Ribosome profiling reveals the rhythmic liver translatome and circadian clock regulation by upstream open reading frames. Genome Research, 25(12), 1848–1859.
Johnson,, C. H., Mori,, T., & Xu,, Y. (2008). A cyanobacterial circadian clockwork. Current Biology, 18(17), R816–R825.
Jordan,, S. D., Kriebs,, A., Vaughan,, M., Duglan,, D., Fan,, W., Henriksson,, E., … Lamia,, K. A. (2017). CRY1/2 selectively repress PPARdelta and limit exercise capacity. Cell Metabolism, 26(1), 243–255.
Jouffe,, C., Cretenet,, G., Symul,, L., Martin,, E., Atger,, F., Naef,, F., & Gachon,, F. (2013). The circadian clock coordinates ribosome biogenesis. PLoS Biology, 11(1), e1001455.
Kaasik,, K., Kivimäe,, S., Allen,, J. J., Chalkley,, R. J., Huang,, Y., Baer,, K., … Fu,, Y. H. (2013). Glucose sensor O‐GlcNAcylation coordinates with phosphorylation to regulate circadian clock. Cell Metabolism, 17(2), 291–302. https://doi.org/10.1016/j.cmet.2012.12.017.
Kato,, Y., Kawamoto,, T., Fujimoto,, K., & Noshiro,, M. (2014). DEC1/STRA13/SHARP2 and DEC2/SHARP1 coordinate physiological processes, including circadian rhythms in response to environmental stimuli. Current Topics in Developmental Biology, 110, 339–372.
Kaufmann,, T., Kukolj,, E., Brachner,, A., Beltzung,, E., Bruno,, M., Kostrhon,, S., … Slade,, D. (2016). SIRT2 regulates nuclear envelope reassembly via ANKLE2 deacetylation. Journal of Cell Science, 129, 4607–4621.
Khapre,, R. V., Kondratova,, A. A., Patel,, S., Dubrovsky,, Y., Wrobel,, M., Antoch,, M. P., & Kondratov,, R. V. (2014). BMAL1‐dependent regulation of the mTOR signaling pathway delays aging. Aging (Albany NY), 6(1), 48–57.
Kim,, Y. H., Marhon,, S. A., Zhang,, Y., Steger,, D. J., Won,, K. J., & Lazar,, M. A. (2018). Rev‐erbalpha dynamically modulates chromatin looping to control circadian gene transcription. Science, 359(6381), 1274.
King,, D. P., Zhao,, Y., Sangoram,, A. M., Wilsbacher,, L. D., Tanaka,, M., Antoch,, M. P., … Takahashi,, J. S. (1997). Positional cloning of the mouse circadian clock gene. Cell, 89(4), 641–653.
Kohsaka,, A., Laposky,, A. D., Ramsey,, K. M., Estrada,, C., Joshu,, C., Kobayashi,, Y., … Bass,, J. (2007). High‐fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metabolism, 6(5), 414–421.
Koike,, N., Yoo,, S. H., Huang,, H. C., Kumar,, V., Lee,, C., Kim,, T. K., & Takahashi,, J. S. (2012). Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science, 338(6105), 349–354.
Kojetin,, D. J., & Burris,, T. P. (2014). REV‐ERB and ROR nuclear receptors as drug targets. Nature Reviews Drug Discovery, 13(3), 197–216.
Kojima,, S., Sher‐Chen,, E. L., & Green,, C. B. (2012). Circadian control of mRNA polyadenylation dynamics regulates rhythmic protein expression. Genes %26 Development, 26(24), 2724–2736.
Konopka,, R. J., & Benzer,, S. (1971). Clock mutants of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 68(9), 2112–2116.
Kornmann,, B., Schaad,, O., Bujard,, H., Takahashi,, J. S., & Schibler,, U. (2007). System‐driven and oscillator‐dependent circadian transcription in mice with a conditionally active liver clock. PLoS Biology, 5(2), e34.
Kowalska,, E., Ripperger,, J. A., Hoegger,, D. C., Bruegger,, P., Buch,, T., Birchler,, T., … Brown,, S. A. (2013). NONO couples the circadian clock to the cell cycle. Proceedings of the National Academy of Sciences of the United States of America, 110(5), 1592–1599.
Kreutz,, C., MacNelly,, S., Follo,, M., Waldin,, A., Binninger‐Lacour,, P., Timmer,, J., & Bartolome‐Rodriguez,, M. M. (2017). Hepatocyte ploidy is a diversity factor for liver homeostasis. Frontiers in Physiology, 8, 862.
Kriebs,, A., Jordan,, S. D., Soto,, E., Henriksson,, E., Sandate,, C. R., Vaughan,, M. E., … Lamia,, K. A. (2017). Circadian repressors CRY1 and CRY2 broadly interact with nuclear receptors and modulate transcriptional activity. Proceedings of the National Academy of Sciences of the United States of America, 114(33), 8776–8781.
Krüger,, M., Moser,, M., Ussar,, S., Thievessen,, I., Luber,, C. A., Forner,, F., … Mann,, M. (2008). SILAC mouse for quantitative proteomics uncovers Kindlin‐3 as an essential factor for red blood cell function. Cell, 134(2), 353–364.
Kume,, K., Zylka,, M. J., Sriram,, S., Shearman,, L. P., Weaver,, D. R., Jin,, X., … Reppert,, S. M. (1999). mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell, 98(2), 193–205.
Kuroda,, H., Tahara,, Y., Saito,, K., Ohnishi,, N., Kubo,, Y., Seo,, Y., … Shibata,, S. (2012). Meal frequency patterns determine the phase of mouse peripheral circadian clocks. Scientific Reports, 2, 711.
Lamia,, K. A., Papp,, S. J., Yu,, R. T., Barish,, G. D., Uhlenhaut,, N. H., Jonker,, J. W., … Evans,, R. M. (2011). Cryptochromes mediate rhythmic repression of the glucocorticoid receptor. Nature, 480(7378), 552–556.
Lamia,, K. A., Sachdeva,, U. M., DiTacchio,, L., Williams,, E. C., Alvarez,, J. G., Egan,, D. F., … Evans,, R. M. (2009). AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science, 326(5951), 437–440.
Lamia,, K. A., Storch,, K. F., & Weitz,, C. J. (2008). Physiological significance of a peripheral tissue circadian clock. Proceedings of the National Academy of Sciences of the United States of America, 105(39), 15172–15177.
Landgraf,, D., Tsang,, A. H., Leliavski,, A., Koch,, C. E., Barclay,, J. L., Drucker,, D. J., & Oster,, H. (2015). Oxyntomodulin regulates resetting of the liver circadian clock by food. eLife, 4, e06253.
Le Martelot,, G., Canella,, D., Symul,, L., Migliavacca,, E., Gilardi,, F., Liechti,, R., … Naef,, F. (2012). Genome‐wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles. PLoS Biology, 10(11), e1001442.
Le Martelot,, G., Claudel,, T., Gatfield,, D., Schaad,, O., Kornmann,, B., Sasso,, G. L., … Schibler,, U. (2009). REV‐ERBalpha participates in circadian SREBP signaling and bile acid homeostasis. PLoS Biology, 7(9), e1000181.
Lee,, C., Etchegaray,, J.‐P., Cagampang,, F. R. A., Loudon,, A. S. I., & Reppert,, S. M. (2001). Posttranslational mechanisms regulate the mammalian circadian clock. Cell, 107(7), 855–867.
Lee,, J., Lee,, Y., Lee,, M. J., Park,, E., Kang,, S. H., Chung,, C. H., … Kim,, K. (2008). Dual modification of BMAL1 by SUMO2/3 and ubiquitin promotes circadian activation of the CLOCK/BMAL1 complex. Molecular and Cellular Biology, 28(19), 6056–6065.
Lee,, J. E., Atkins,, N., Jr., Hatcher,, N. G., Zamdborg,, L., Gillette,, M. U., Sweedler,, J. V., & Kelleher,, N. L. (2010). Endogenous peptide discovery of the rat circadian clock: A focused study of the suprachiasmatic nucleus by ultrahigh performance tandem mass spectrometry. Molecular %26 Cellular Proteomics, 9(2), 285–297.
Lee,, J. E., Zamdborg,, L., Southey,, B. R., Atkins,, N., Jr., Mitchell,, J. W., Li,, M., … Sweedler,, J. V. (2013). Quantitative peptidomics for discovery of circadian‐related peptides from the rat suprachiasmatic nucleus. Journal of Proteome Research, 12(2), 585–593.
Li,, M.‐D., Ruan,, H.‐B., Hughes,, M. E., Lee,, J.‐S., Singh,, J. P., Jones,, S. P., … Yang,, X. (2013). O‐GlcNAc signaling entrains the circadian CLOCK by inhibiting BMAL1/CLOCK Ubiquitination. Cell Metabolism, 17(2), 303–310.
Li,, S., Wang,, M., Ao,, X., Chang,, A. K., Yang,, C., Zhao,, F., … Wu,, H. (2013). CLOCK is a substrate of SUMO and sumoylation of CLOCK upregulates the transcriptional activity of estrogen receptor‐alpha. Oncogene, 32(41), 4883–4891.
Liu,, Y., Hu,, W., Murakawa,, Y., Yin,, J., Wang,, G., Landthaler,, M., & Yan,, J. (2013). Cold‐induced RNA‐binding proteins regulate circadian gene expression by controlling alternative polyadenylation. Scientific Reports, 3, 2054.
Luciano,, A. K., Zhou,, W., Santana,, J. M., Kyriakides,, C., Velazquez,, H., & Sessa,, W. C. (2018). CLOCK phosphorylation by AKT regulates its nuclear accumulation and circadian gene expression in peripheral tissues. The Journal of Biological Chemistry, 293(23), 9126–9136.
Luck,, S., Thurley,, K., Thaben,, P. F., & Westermark,, P. O. (2014). Rhythmic degradation explains and unifies circadian transcriptome and proteome data. Cell Reports, 9(2), 741–751.
Mange,, F., Praz,, V., Migliavacca,, E., Willis,, I. M., Schutz,, F., Hernandez,, N., & Cycli,, X. C. (2017). Diurnal regulation of RNA polymerase III transcription is under the control of both the feeding‐fasting response and the circadian clock. Genome Research, 27(6), 973–984.
Marcheva,, B., Ramsey,, K. M., Buhr,, E. D., Kobayashi,, Y., Su,, H., Ko,, C. H., … Bass,, J. (2010). Disruption of the CLOCK components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature, 466(7306), 627–631.
Martino,, T. A., Tata,, N., Bjarnason,, G. A., Straume,, M., & Sole,, M. J. (2007). Diurnal protein expression in blood revealed by high throughput mass spectrometry proteomics and implications for translational medicine and body time of day. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 293(3), R1430–R1437.
Masri,, S., Patel,, V. R., Eckel‐Mahan,, K. L., Peleg,, S., Forne,, I., Ladurner,, A. G., … Sassone‐Corsi,, P. (2013). Circadian acetylome reveals regulation of mitochondrial metabolic pathways. Proceedings of the National Academy of Sciences of the United States of America, 110(9), 3339–3344.
Masri,, S., Rigor,, P., Cervantes,, M., Ceglia,, N., Sebastian,, C., Xiao,, C., … Sassone‐Corsi,, P. (2014). Partitioning circadian transcription by SIRT6 leads to segregated control of cellular metabolism. Cell, 158(3), 659–672.
Matsumoto,, E., Ishihara,, A., Tamai,, S., Nemoto,, A., Iwase,, K., Hiwasa,, T., … Takiguchi,, M. (2010). Time of day and nutrients in feeding govern daily expression rhythms of the gene for sterol regulatory element‐binding protein (SREBP)‐1 in the mouse liver. Journal of Biological Chemistry, 285(43), 33028–33036.
Mauvoisin,, D., Atger,, F., Dayon,, L., Núñez Galindo,, A., Wang,, J., Martin,, E., … Gachon,, F. (2017). Circadian and feeding rhythms orchestrate the diurnal liver Acetylome. Cell Reports, 20(7), 1729–1743.
Mauvoisin,, D., Wang,, J., Jouffe,, C., Martin,, E., Atger,, F., Waridel,, P., … Naef,, F. (2014). Circadian clock‐dependent and ‐independent rhythmic proteomes implement distinct diurnal functions in mouse liver. Proceedings of the National Academy of Sciences of the United States of America, 111(1), 167–172.
Mendoza‐Viveros,, L., Chiang,, C. K., Ong,, J. L. K., Hegazi,, S., Cheng,, A. H., Bouchard‐Cannon,, P., … Cheng,, H. M. (2017). miR‐132/212 modulates seasonal adaptation and dendritic morphology of the central circadian clock. Cell Reports, 19(3), 505–520.
Menet,, J. S., Rodriguez,, J., Abruzzi,, K. C., & Rosbash,, M. (2012). Nascent‐Seq reveals novel features of mouse circadian transcriptional regulation. eLife, 1, e00011.
Mermet,, J., Yeung,, J., Hurni,, C., Mauvoisin,, D., Gustafson,, K., Jouffe,, C., … Naef,, F. (2018). Clock‐dependent chromatin topology modulates circadian transcription and behavior. Genes %26 Development, 32(5–6), 347–358.
Moller,, M., Rath,, M. F., Ludvigsen,, M., Honore,, B., & Vorum,, H. (2017). Diurnal expression of proteins in the retina of the blind cone‐rod homeobox (Crx(‐/‐)) mouse and the 129/Sv mouse: A proteomic study. Acta Ophthalmologica, 95(7), 717–726.
Moller,, M., Sparre,, T., Bache,, N., Roepstorff,, P., & Vorum,, H. (2007). Proteomic analysis of day‐night variations in protein levels in the rat pineal gland. Proteomics, 7(12), 2009–2018.
Moore,, R. Y., & Eichler,, V. B. (1972). Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Research, 42(1), 201–206.
Nader,, N., Chrousos,, G. P., & Kino,, T. (2009). Circadian rhythm transcription factor CLOCK regulates the transcriptional activity of the glucocorticoid receptor by acetylating its hinge region lysine cluster: Potential physiological implications. The FASEB Journal, 23(5), 1572–1583.
Nagoshi,, E., Brown,, S. A., Dibner,, C., Kornmann,, B., & Schibler,, U. (2005). Circadian gene expression in cultured cells. Methods in Enzymology, 393, 543–557.
Nakahata,, Y., Kaluzova,, M., Grimaldi,, B., Sahar,, S., Hirayama,, J., Chen,, D., … Sassone‐Corsi,, P. (2008). The NAD+‐dependent deacetylase SIRT1 modulates CLOCK‐mediated chromatin remodeling and circadian control. Cell, 134(2), 329–340.
Nakahata,, Y., Sahar,, S., Astarita,, G., Kaluzova,, M., & Sassone‐Corsi,, P. (2009). Circadian control of the NAD⁺ salvage pathway by CLOCK‐SIRT1. Science, 324(5927), 654–657.
Narumi,, R., Shimizu,, Y., Ukai‐Tadenuma,, M., Ode,, K. L., Kanda,, G. N., Shinohara,, Y., … Ueda,, H. R. (2016). Mass spectrometry‐based absolute quantification reveals rhythmic variation of mouse circadian clock proteins. Proceedings of the National Academy of Sciences of the United States of America, 113, E3461–E3467.
Neufeld‐Cohen,, A., Robles,, M. S., Aviram,, R., Manella,, G., Adamovich,, Y., Ladeuix,, B., … Asher,, G. (2016). Circadian control of oscillations in mitochondrial rate‐limiting enzymes and nutrient utilization by PERIOD proteins. Proceedings of the National Academy of Sciences of the United States of America, 113, E1673–E1682.
O`Neill,, J. S., & Reddy,, A. B. (2011). Circadian clocks in human red blood cells. Nature, 469(7331), 498–503.
O`Neill,, J. S., van Ooijen,, G., Dixon,, L. E., Troein,, C., Corellou,, F., Bouget,, F. Y., … Millar,, A. J. (2011). Circadian rhythms persist without transcription in a eukaryote. Nature, 469(7331), 554–558.
Ohno,, T., Onishi,, Y., & Ishida,, N. (2007). The negative transcription factor E4BP4 is associated with circadian clock protein PERIOD2. Biochemical and Biophysical Research Communications, 354(4), 1010–1015.
Ong,, S. E., & Mann,, M. (2005). Mass spectrometry‐based proteomics turns quantitative. Nature Chemical Biology, 1(5), 252–262.
Oosterman,, J. E., Kalsbeek,, A., la Fleur,, S. E., & Belsham,, D. D. (2015). Impact of nutrients on circadian rhythmicity. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 308(5), R337–R350.
Panda,, S., Antoch,, M. P., Miller,, B. H., Su,, A. I., Schook,, A. B., Straume,, M., … Hogenesch,, J. B. (2002). Coordinated transcription of key pathways in the mouse by the circadian clock. Cell, 109(3), 307–320.
Paschos,, G. K., Ibrahim,, S., Song,, W. L., Kunieda,, T., Grant,, G., Reyes,, T. M., … Fitzgerald,, G. A. (2012). Obesity in mice with adipocyte‐specific deletion of clock component Arntl. Nature Medicine, 18(12), 1768–1777.
Peek,, C. B., Affinati,, A. H., Ramsey,, K. M., Kuo,, H. Y., Yu,, W., Sena,, L. A., … Bass,, J. (2013). Circadian clock NAD+ cycle drives mitochondrial oxidative metabolism in mice. Science, 342(6158), 1243417.
Pircher,, P., Chomez,, P., Yu,, F., Vennstrom,, B., & Larsson,, L. (2005). Aberrant expression of myosin isoforms in skeletal muscles from mice lacking the rev‐erbAalpha orphan receptor gene. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 288(2), R482–R490.
Podobed,, P., Pyle,, W. G., Ackloo,, S., Alibhai,, F. J., Tsimakouridze,, E. V., Ratcliffe,, W. F., … Martino,, T. A. (2014). The day/night proteome in the murine heart. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 307, R121–R137.
Preitner,, N., Damiola,, F., Lopez‐Molina,, L., Zakany,, J., Duboule,, D., Albrecht,, U., & Schibler,, U. (2002). The orphan nuclear receptor REV‐ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell, 110(2), 251–260.
Preussner,, M., & Heyd,, F. (2016). Post‐transcriptional control of the mammalian circadian clock: Implications for health and disease. Pflügers Archiv, 468(6), 983–991.
Preussner,, M., Wilhelmi,, I., Schultz,, A. S., Finkernagel,, F., Michel,, M., Moroy,, T., & Heyd,, F. (2014). Rhythmic U2af26 alternative splicing controls PERIOD1 stability and the circadian clock in mice. Molecular Cell, 54(4), 651–662.
Ralph,, M. R., Foster,, R. G., Davis,, F. C., & Menaker,, M. (1990). Transplanted suprachiasmatic nucleus determines circadian period. Science, 247(4945), 975–978.
Ramanathan,, C., Kathale,, N. D., Liu,, D., Lee,, C., Freeman,, D. A., Hogenesch,, J. B., … Liu,, A. C. (2018). mTOR signaling regulates central and peripheral circadian clock function. PLoS Genetics, 14(5), e1007369.
Ramsey,, K. M., Yoshino,, J., Brace,, C. S., Abrassart,, D., Kobayashi,, Y., Marcheva,, B., … Bass,, J. (2009). Circadian clock feedback cycle through NAMPT‐mediated NAD+ biosynthesis. Science, 324(5927), 651–654.
Reddy,, A. B., Karp,, N. A., Maywood,, E. S., Sage,, E. A., Deery,, M., O`Neill,, J. S., … Hastings,, M. H. (2006). Circadian orchestration of the hepatic proteome. Current Biology, 16(11), 1107–1115.
Reischl,, S., & Kramer,, A. (2011). Kinases and phosphatases in the mammalian circadian clock. FEBS Letters, 585(10), 1393–1399.
Reppert,, S. M., & Weaver,, D. R. (2001). Molecular analysis of mammalian circadian rhythms. Annual Review of Physiology, 63, 647–676.
Rey,, G., Milev,, N. B., Valekunja,, U. K., Ch,, R., Ray,, S., Silva Dos Santos,, M., … Reddy,, A. B. (2018). Metabolic oscillations on the circadian time scale in Drosophila cells lacking clock genes. Molecular Systems Biology, 14(8), e8376.
Rey,, G., Valekunja,, U. K., Feeney,, K. A., Wulund,, L., Milev,, N. B., Stangherlin,, A., … Reddy,, A. B. (2016). The pentose phosphate pathway regulates the circadian clock. Cell Metabolism, 24(3), 462–473.
Ringel,, A. E., Tucker,, S. A., & Haigis,, M. C. (2018). Chemical and physiological features of mitochondrial acylation. Molecular Cell, 72(4), 610–624.
Robles,, M. S., Cox,, J., & Mann,, M. (2014). In‐vivo quantitative proteomics reveals a key contribution of post‐transcriptional mechanisms to the circadian regulation of liver metabolism. PLoS Genetics, 10(1), e1004047.
Robles,, M. S., Humphrey,, S. J., & Mann,, M. (2017). Phosphorylation is a central mechanism for circadian control of metabolism and physiology. Cell Metabolism, 25(1), 118–127.
Rudic,, R. D., McNamara,, P., Curtis,, A.‐M., Boston,, R. C., Panda,, S., Hogenesch,, J. B., & FitzGerald,, G. A. (2004). BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biology, 2(11), e377.
Rutter,, J., Reick,, M., Wu,, L. C., & McKnight,, S. L. (2001). Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science, 293(5529), 510–514.
Sadacca,, L. A., Lamia,, K. A., deLemos,, A. S., Blum,, B., & Weitz,, C. J. (2011). An intrinsic circadian clock of the pancreas is required for normal insulin release and glucose homeostasis in mice. Diabetologia, 54(1), 120–124.
Sahasrabuddhe,, N. A., Huang,, T.‐C., Kumar,, P., Yang,, Y., Ghosh,, B., Leach,, S. D., … Pandey,, A. (2015). Ablation of dicer leads to widespread perturbation of signaling pathways. Biochemical and Biophysical Research Communications, 463(3), 389–394.
Sahasrabuddhe,, N. A., Huang,, T. C., Ahmad,, S., Kim,, M. S., Yang,, Y., Ghosh,, B., … Pandey,, A. (2014). Regulation of PPAR‐alpha pathway by dicer revealed through proteomic analysis. Journal of Proteomics, 108, 306–315.
Sancar,, A., Lindsey‐Boltz,, L. A., Kang,, T. H., Reardon,, J. T., Lee,, J. H., & Ozturk,, N. (2010). Circadian clock control of the cellular response to DNA damage. FEBS Letters, 584(12), 2618–2625.
Sato,, F., Kohsaka,, A., Bhawal,, U. K., & Muragaki,, Y. (2018). Potential roles of Dec and Bmal1 genes in interconnecting circadian clock and energy metabolism. International Journal of Molecular Sciences, 19(3). https://doi.org/10.3390/ijms19030781
Sato,, T. K., Panda,, S., Miraglia,, L. J., Reyes,, T. M., Rudic,, R. D., McNamara,, P., … Hogenesch,, J. B. (2004). A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron, 43(4), 527–537.
Schmitt,, K., Grimm,, A., Dallmann,, R., Oettinghaus,, B., Restelli,, L. M., Witzig,, M., … Eckert,, A. (2018). Circadian control of DRP1 activity regulates mitochondrial dynamics and bioenergetics. Cell Metabolism, 27, 1–10.
Shearman,, L. P., Zylka,, M. J., Weaver,, D. R., Kolakowski,, L. F., Jr., & Reppert,, S. M. (1997). Two period homologs: Circadian expression and photic regulation in the suprachiasmatic nuclei. Neuron, 19(6), 1261–1269.
Shimba,, S., Ishii,, N., Ohta,, Y., Ohno,, T., Watabe,, Y., Hayashi,, M., … Tezuka,, M. (2005). Brain and muscle Arnt‐like protein‐1 (BMAL1), a component of the molecular clock, regulates adipogenesis. Proceedings of the National Academy of Sciences of the United States of America, 102(34), 12071–12076.
Shin,, J., He,, M., Liu,, Y., Paredes,, S., Villanova,, L., Brown,, K., … Chen,, D. (2013). SIRT7 represses Myc activity to suppress ER stress and prevent fatty liver disease. Cell Reports, 5(3), 654–665.
Stephan,, F. K., & Zucker,, I. (1972). Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proceedings of the National Academy of Sciences of the United States of America, 69(6), 1583–1586.
Stokkan,, K. A., Yamazaki,, S., Tei,, H., Sakaki,, Y., & Menaker,, M. (2001). Entrainment of the circadian clock in the liver by feeding. Science, 291(5503), 490–493.
Storch,, K. F., Paz,, C., Signorovitch,, J., Raviola,, E., Pawlyk,, B., Li,, T., & Weitz,, C. J. (2007). Intrinsic circadian clock of the mammalian retina: Importance for retinal processing of visual information. Cell, 130(4), 730–741.
Stubblefield,, J. J., Gao,, P., Kilaru,, G., Mukadam,, B., Terrien,, J., & Green,, C. B. (2018). Temporal control of metabolic amplitude by nocturnin. Cell Reports, 22(5), 1225–1235.
Subramanian,, P., Jayapalan,, J. J., Abdul‐Rahman,, P. S., Arumugam,, M., & Hashim,, O. H. (2016). Temporal regulation of proteome profile in the fruit fly, Drosophila melanogaster. PeerJ, 4, e2080.
Szabo,, A., Papin,, C., Cornu,, D., Chelot,, E., Lipinszki,, Z., Udvardy,, A., … Rouyer,, F. (2018). Ubiquitylation dynamics of the clock cell proteome and TIMELESS during a circadian cycle. Cell Reports, 23(8), 2273–2282.
Takahashi,, J. S. (2017). Transcriptional architecture of the mammalian circadian clock. Nature Reviews Genetics, 18(3), 164–179.
Tannu,, N. S., & Hemby,, S. E. (2006). Two‐dimensional fluorescence difference gel electrophoresis for comparative proteomics profiling. Nature Protocols, 1(4), 1732–1742.
Tei,, H., Okamura,, H., Shigeyoshi,, Y., Fukuhara,, C., Ozawa,, R., Hirose,, M., & Sakaki,, Y. (1997). Circadian oscillation of a mammalian homologue of the Drosophila period gene. Nature, 389(6650), 512–516.
Tian,, R., Alvarez‐Saavedra,, M., Cheng,, H. Y., & Figeys,, D. (2011). Uncovering the proteome response of the master circadian clock to light using an AutoProteome system. Molecular %26 Cellular Proteomics, 10(11), M110.007252.
Tong,, Z., Wang,, M., Wang,, Y., Kim,, D. D., Grenier,, J. K., Cao,, J., … Lin,, H. (2017). SIRT7 is an RNA‐activated protein lysine deacylase. ACS Chemical Biology, 12(1), 300–310.
Torres,, M., Becquet,, D., Franc,, J. L., & Francois‐Bellan,, A. M. (2018). Circadian processes in the RNA life cycle. WIREs RNA, 9(3), e1467.
Tsuchiya,, Y., Minami,, I., Kadotani,, H., Todo,, T., & Nishida,, E. (2013). Circadian clock‐controlled diurnal oscillation of Ras/ERK signaling in mouse liver. Proceedings of the Japan Academy, Series B, 89(1), 59–65.
Tsuji,, T., Hirota,, T., Takemori,, N., Komori,, N., Yoshitane,, H., Fukuda,, M., … Fukada,, Y. (2007). Circadian proteomics of the mouse retina. Proteomics, 7(19), 3500–3508.
Tulsian,, R., Velingkaar,, N., & Kondratov,, R. (2018). Caloric restriction effects on liver mTOR signaling are time‐of‐day dependent. Aging, 10(7), 1640–1648.
Ueda,, H. R., Hayashi,, S., Chen,, W., Sano,, M., Machida,, M., Shigeyoshi,, Y., … Hashimoto,, S. (2005). System‐level identification of transcriptional circuits underlying mammalian circadian clocks. Nature Genetics, 37(2), 187–192.
Um,, J. H., Yang,, S., Yamazaki,, S., Kang,, H., Viollet,, B., Foretz,, M., & Chung,, J. H. (2007). Activation of 5`‐AMP‐activated kinase with diabetes drug metformin induces casein kinase Iepsilon (CKIepsilon)‐dependent degradation of clock protein mPer2. The Journal of Biological Chemistry, 282(29), 20794–20798.
van der Horst,, G. T., Muijtjens,, M., Kobayashi,, K., Takano,, R., Kanno,, S., Takao,, M., … Yasui,, A. (1999). Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature, 398(6728), 627–630.
van der Veen,, D. R., Minh,, N. L., Gos,, P., Arneric,, M., Gerkema,, M. P., & Schibler,, U. (2006). Impact of behavior on central and peripheral circadian clocks in the common vole Microtus arvalis, a mammal with ultradian rhythms. Proceedings of the National Academy of Sciences of the United States of America, 103(9), 3393.
Vollmers,, C., Gill,, S., DiTacchio,, L., Pulivarthy,, S. R., Le,, H. D., & Panda,, S. (2009). Time of feeding and the intrinsic circadian clock drive rhythms in hepatic gene expression. Proceedings of the National Academy of Sciences of the United States of America, 106(50), 21453–21458.
Vollmers,, C., Schmitz,, R. J., Nathanson,, J., Yeo,, G., Ecker,, J. R., & Panda,, S. (2012). Circadian oscillations of protein‐coding and regulatory RNAs in a highly dynamic mammalian liver epigenome. Cell Metabolism, 16(6), 833–845.
Walsh,, C. T., Garneau‐Tsodikova,, S., & Gatto,, G. J., Jr. (2005). Protein posttranslational modifications: The chemistry of proteome diversifications. Angewandte Chemie (International Ed. in English), 44(45), 7342–7372.
Wang,, J., Mauvoisin,, D., Martin,, E., Atger,, F., Galindo,, A. N., Dayon,, L., … Gachon,, F. (2017). Nuclear proteomics uncovers diurnal regulatory landscapes in mouse liver. Cell Metabolism, 25(1), 102–117.
Wang,, J., Symul,, L., Yeung,, J., Gobet,, C., Sobel,, J., Luck,, S., … Naef,, F. (2018). Circadian clock‐dependent and ‐independent posttranscriptional regulation underlies temporal mRNA accumulation in mouse liver. Proceedings of the National Academy of Sciences of the United States of America, 115(8), E1916–E1925.
Wang,, Y., Song,, L., Liu,, M., Ge,, R., Zhou,, Q., Liu,, W., … Ding,, C. (2018). A proteomics landscape of circadian clock in mouse liver. Nature Communications, 9(1), 1553.
Wang,, Y. P., Zhou,, L. S., Zhao,, Y. Z., Wang,, S. W., Chen,, L. L., Liu,, L. X., … Ye,, D. (2014). Regulation of G6PD acetylation by SIRT2 and KAT9 modulates NADPH homeostasis and cell survival during oxidative stress. The EMBO Journal, 33(12), 1304–1320.
Wang,, Z., Ma,, J., Miyoshi,, C., Li,, Y., Sato,, M., Ogawa,, Y., … Liu,, Q. (2018). Quantitative phosphoproteomic analysis of the molecular substrates of sleep need. Nature, 558(7710), 435–439.
Welsh,, D. K., Yoo,, S. H., Liu,, A. C., Takahashi,, J. S., & Kay,, S. A. (2004). Bioluminescence imaging of individual fibroblasts reveals persistent, independently phased circadian rhythms of clock gene expression. Current Biology, 14(24), 2289–2295.
Wible,, R. S., Ramanathan,, C., Sutter,, C. H., Olesen,, K. M., Kensler,, T. W., Liu,, A. C., & Sutter,, T. R. (2018). NRF2 regulates core and stabilizing circadian clock loops, coupling redox and timekeeping in Mus musculus. eLife, 7, e31656.
Yamaguchi,, S., Mitsui,, S., Yan,, L., Yagita,, K., Miyake,, S., & Okamura,, H. (2000). Role of DBP in the circadian oscillatory mechanism. Molecular and Cellular Biology, 20(13), 4773–4781.
Yamajuku,, D., Inagaki,, T., Haruma,, T., Okubo,, S., Kataoka,, Y., Kobayashi,, S., … Oda,, H. (2012). Real‐time monitoring in three‐dimensional hepatocytes reveals that insulin acts as a synchronizer for liver clock. Scientific Reports, 2, 439.
Yin,, L., Wu,, N., Curtin,, J. C., Qatanani,, M., Szwergold,, N. R., Reid,, R. A., … Lazar,, M. A. (2007). Rev‐erbalpha, a heme sensor that coordinates metabolic and circadian pathways. Science, 318(5857), 1786–1789.
Zehring,, W. A., Wheeler,, D. A., Reddy,, P., Konopka,, R. J., Kyriacou,, C. P., Rosbash,, M., & Hall,, J. C. (1984). P‐element transformation with period locus DNA restores rhythmicity to mutant, arrhythmic Drosophila melanogaster. Cell, 39(2 Pt 1), 369–376.
Zhang,, E. E., Liu,, Y., Dentin,, R., Pongsawakul,, P. Y., Liu,, A. C., Hirota,, T., … Kay,, S. A. (2010). Cryptochrome mediates circadian regulation of cAMP signaling and hepatic gluconeogenesis. Nature Medicine, 16(10), 1152–1156.
Zhang,, R., Lahens,, N. F., Ballance,, H. I., Hughes,, M. E., & Hogenesch,, J. B. (2014). A circadian gene expression atlas in mammals: Implications for biology and medicine. Proceedings of the National Academy of Sciences of the United States of America, 111(45), 16219–16224.
Zhong,, X., Yu,, J., Frazier,, K., Weng,, X., Li,, Y., Cham,, C. M., … Leone,, V. (2018). Circadian clock regulation of hepatic lipid metabolism by modulation of m(6)A mRNA methylation. Cell Reports, 25(7), 1816–1828.
Zhu,, H., Tamura,, T., & Hamachi,, I. (2019). Chemical proteomics for subcellular proteome analysis. Current Opinion in Chemical Biology, 48, 1–7.
Zylka,, M. J., Shearman,, L. P., Weaver,, D. R., & Reppert,, S. M. (1998). Three period homologs in mammals: Differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron, 20(6), 1103–1110.

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