Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

A Time to Fast, a Time to Feast: The Crosstalk between Metabolism and the Circadian Clock

  • Kovac, Judit (Circadian Rhythms Group, Max Planck Institute of Biophysical Chemistry) ;
  • Husse, Jana (Genes and Behaviour Department, Max Planck Institute of Biophysical Chemistry) ;
  • Oster, Henrik (Circadian Rhythms Group, Max Planck Institute of Biophysical Chemistry)
  • Received : 2009.07.08
  • Accepted : 2009.07.11
  • Published : 2009.08.31
⟨ Previous Next ⟩

Abstract

The cyclic environmental conditions brought about by the 24 h rotation of the earth have allowed the evolution of endogenous circadian clocks that control the temporal alignment of behaviour and physiology, including the uptake and processing of nutrients. Both metabolic and circadian regulatory systems are built upon a complex feedback network connecting centres of the central nervous system and different peripheral tissues. Emerging evidence suggests that circadian clock function is closely linked to metabolic homeostasis and that rhythm disruption can contribute to the development of metabolic disease. At the same time, metabolic processes feed back into the circadian clock, affecting clock gene expression and timing of behaviour. In this review, we summarize the experimental evidence for this bimodal interaction, with a focus on the molecular mechanisms mediating this exchange, and outline the implications for clock-based and metabolic diseases.

Keywords

Acknowledgement

Supported by : German Research Council (DFG)

References

  1. Ando, H., Yanagihara, H., Hayashi, Y., Obi, Y., Tsuruoka, S., Takamura, T., Kaneko, S., and Fujimura, A. (2005). Rhythmic messenger ribonucleic acid expression of clock genes and adipocytokines in mouse visceral adipose tissue. Endocrinology 146, 5631-5636 https://doi.org/10.1210/en.2005-0771
  2. Balsalobre, A., Brown, S.A., Marcacci, L., Tronche, F., Kellendonk, C., Reichardt, H.M., Schutz, G., and Schibler, U. (2000). Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289, 2344-2347 https://doi.org/10.1126/science.289.5488.2344
  3. Bray, M.S., and Young, M.E. (2007). Circadian rhythms in the development of obesity: potential role for the circadian clock within the adipocyte. Obes. Rev.8, 169-181 https://doi.org/10.1111/j.1467-789X.2006.00277.x
  4. Bray, M.S., Shaw, C.A., Moore, M.W.S., Garcia, R.A.P., Zanquetta, M.M., Durgan, D.J., Jeong, W.J., Tsai, J.-Y., Bugger, H., Zhang, D.I= et alK (2008). Disruption of the circadian clock within the cardiomyocyte influences myocardial contractile function, metabolism, and gene expression. Am. J. Physiol. Heart Circ. Physiol. 294, H1036-1047 https://doi.org/10.1152/ajpheart.01291.2007
  5. Buijs, R.M., Scheer, F.A., Kreier, F., Yi, C., Bos, N., Goncharuk, V.D., and Kalsbeek, A. (2006). Organization of circadian functions: interaction with the body. Prog. Brain Res. 153, 341-360 https://doi.org/10.1016/S0079-6123(06)53020-1
  6. Canaple, L., Rambaud, J., Dkhissi-Benyahya, O., Rayet, B., Tan, N.S., Michalik, L., Delaunay, F., Wahli, W., and Laudet, V. (2006). Reciprocal regulation of brain and muscle Arnt-like protein 1 and peroxisome proliferator-activated receptor alpha defines a novel positive feedback loop in the rodent liver circadian clock. Mol. Endocrinol. 20, 1715-1727 https://doi.org/10.1210/me.2006-0052
  7. Damiola, F., Le Minh, N., Preitner, N., Kornmann, B., Fleury-Olela, F., and Schibler, U. (2000). Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 14, 2950-2961 https://doi.org/10.1101/gad.183500
  8. Dioum, E.M., Rutter, J., Tuckerman, J.R., Gonzalez, G., Gilles-Gonzalez, M.A., and McKnight, S.L. (2002). NPAS2: a gasresponsive transcription factor. Science 298, 2385-2387 https://doi.org/10.1126/science.1078456
  9. Duffield, G.E. (2003). DNA microarray analyses of circadian timing: the genomic basis of biological time. J. Neuroendocrinol. 15, 991-1002 https://doi.org/10.1046/j.1365-2826.2003.01082.x
  10. Fontaine, C., Dubois, G., Duguay, Y., Helledie, T., Vu-Dac, N., Gervois, P., Soncin, F., Mandrup, S., Fruchart, J.C., Fruchart- Najib, J.I= et alK (2003). The orphan nuclear receptor Rev- Erbalpha is a peroxisome proliferator-activated receptor (PPAR) gamma target gene and promotes PPARgamma-induced adipocyte differentiation. J. Biol. Chem. 278, 37672-37680 https://doi.org/10.1074/jbc.M304664200
  11. Foster, R.G., and Hankins, M.W. (2007). Circadian vision. Curr. Biol. 17, R746-751 https://doi.org/10.1016/j.cub.2007.07.007
  12. Gervois, P., Chopin-Delannoy, S., Fadel, A., Dubois, G., Kosykh, V., Fruchart, J.C., Najib, J., Laudet, V., and Staels, B. (1999). Fibrates increase human REV-ERBalpha expression in liver via a novel peroxisome proliferator-activated receptor response element. Mol. Endocrinol. 13, 400-409 https://doi.org/10.1210/me.13.3.400
  13. Goh, B.C., Wu, X., Evans, A.E., Johnson, M.L., Hill, M.R., and Gimble, J.M. (2007). Food entrainment of circadian gene expression altered in PPARalpha-/- brown fat and heart. Biochem. Biophys. Res. Commun. 360, 828-833 https://doi.org/10.1016/j.bbrc.2007.06.136
  14. Green, C.B., Takahashi, J.S., and Bass, J. (2008). The meter of metabolism. Cell 134, 728-742 https://doi.org/10.1016/j.cell.2008.08.022
  15. Harmer, S.L., Panda, S., and Kay, S.A. (2001). Molecular bases of circadian rhythms. Annu. Rev. Cell Dev. Biol. 17, 215-253 https://doi.org/10.1146/annurev.cellbio.17.1.215
  16. Inoue, I., Shinoda, Y., Ikeda, M., Hayashi, K., Kanazawa, K., Nomura, M., Matsunaga, T., Xu, H., Kawai, S., Awata, T.I=et alK (2005). CLOCK/BMAL1 is involved in lipid metabolism via transactivation of the peroxisome proliferator-activated receptor (PPAR) response element. J. Atheroscler. Thromb. 12, 169-174 https://doi.org/10.5551/jat.12.169
  17. Ishida, A., Mutoh, T., Ueyama, T., Bando, H., Masubuchi, S., Nakahara, D., Tsujimoto, G., and Okamura, H. (2005). Light activates the adrenal gland: timing of gene expression and glucocorticoid release. Cell Metab. 2, 297-307 https://doi.org/10.1016/j.cmet.2005.09.009
  18. Kaasik, K., and Lee, C.C. (2004). Reciprocal regulation of haem biosynthesis and the circadian clock in mammals. Nature 430, 467-471 https://doi.org/10.1038/nature02724
  19. Kaneko, K., Yamada, T., Tsukita, S., Takahashi, K., Ishigaki, Y., Oka, Y., and Katagiri, H. (2009). Obesity alters circadian expressions of molecular clock genes in the brainstem. Brain Res. 1263, 58-68 https://doi.org/10.1016/j.brainres.2008.12.071
  20. Kawamoto, T., Noshiro, M., Furukawa, M., Honda, K.K., Nakashima, A., Ueshima, T., Usui, E., Katsura, Y., Fujimoto, K., Honma, S., et al. (2006). Effects of fasting and re-feeding on the expression of Dec1, Per1, and other clock-related genes. J. Biochem. 140, 401-408 https://doi.org/10.1093/jb/mvj165
  21. Ko, C.H., and Takahashi, J.S. (2006). Molecular components of the mammalian circadian clock. Hum. Mol. Genet. 15, R271-277 https://doi.org/10.1093/hmg/ddl207
  22. Kohsaka, A., Laposky, A.D., Ramsey, K.M., Estrada, C., Joshu, C., Kobayashi, Y., Turek, F.W., and Bass, J. (2007). High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab. 6, 414-421 https://doi.org/10.1016/j.cmet.2007.09.006
  23. Kondratov, R.V., Kondratova, A.A., Gorbacheva, V.Y., Vykhovanets, O.V., and Antoch, M.P. (2006). Early aging and age-related pathologies in mice deficient in BMAL1, the core componentof the circadian clock. Genes Dev. 20, 1868-1873 https://doi.org/10.1101/gad.1432206
  24. Lamia, K.A., Storch, K.-F., and Weitz, C.J. (2008). Physiological significance of a peripheral tissue circadian clock. Proc. Natl. Acad. Sci. USA 105, 15172-15177 https://doi.org/10.1073/pnas.0806717105
  25. Laposky, A.D., Shelton, J., Bass, J., Dugovic, C., Perrino, N., and Turek, F.W. (2006). Altered sleep regulation in leptin-deficient mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R894-903 https://doi.org/10.1152/ajpregu.00304.2005
  26. Laposky, A.D., Bass, J., Kohsaka, A., and Turek, F.W. (2008). Sleep and circadian rhythms: key components in the regulation of energy metabolism. FEBS Lett. 582, 142-151 https://doi.org/10.1016/j.febslet.2007.06.079
  27. Lau, P., Nixon, S.J., Parton, R.G., and Muscat, G.E. (2004). RORalpha regulates the expression of genes involved in lipid homeostasis in skeletal muscle cells: caveolin-3 and CPT-1 are direct targets of ROR. J. Biol. Chem. 279, 36828-36840 https://doi.org/10.1074/jbc.M404927200
  28. Le Minh, N., Damiola, F., Tronche, F., Schutz, G., and Schibler, U. (2001). Glucocorticoid hormones inhibit food-induced phaseshifting of peripheral circadian oscillators. EMBO J. 20, 7128-7136 https://doi.org/10.1093/emboj/20.24.7128
  29. Lefebvre, P., Chinetti, G., Fruchart, J.C., and Staels, B. (2006). Sorting out the roles of PPAR alpha in energy metabolism and vascular homeostasis. J. Clin. Invest. 116, 571-580 https://doi.org/10.1172/JCI27989
  30. Levi, F., and Schibler, U. (2007). Circadian rhythms: mechanisms and therapeutic implications. Annu. Rev. Pharmacol. Toxicol. 47, 593-628 https://doi.org/10.1146/annurev.pharmtox.47.120505.105208
  31. Lin, J., Handschin, C., and Spiegelman, B.M. (2005). Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 1, 361-370 https://doi.org/10.1016/j.cmet.2005.05.004
  32. Liu, C., Li, S., Liu, T., Borjigin, J., and Lin, J.D. (2007). Transcriptional coactivator PGC-1alpha integrates the mammalian clock and energy metabolism. Nature 447, 477-481 https://doi.org/10.1038/nature05767
  33. Michael, T.P., Salome, P.A., Yu, H.J., Spencer, T.R., Sharp, E.L., McPeek, M.A., Alonso, J.M., Ecker, J.R., and McClung, C.R. (2003). Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302, 1049-1053 https://doi.org/10.1126/science.1082971
  34. Mistlberger, R.E. (2005). Circadian regulation of sleep in mammals: Role of the suprachiasmatic nucleus. Brain Res. Rev. 49, 429-454 https://doi.org/10.1016/j.brainresrev.2005.01.005
  35. Nakahata, Y., Sahar, S., Astarita, G., Kaluzova, M., and Sassone-Corsi, P. (2009). Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science 324, 654-657 https://doi.org/10.1126/science.1170803
  36. Oster, H., and Foster, R.G. (2008). The interaction of light and the circadian clock network - a new therapeutic approach for the treatment of neuropsychiatric disorders? In Progress in Circadian Rhythms Research, A.-L. Leglise, ed. (Hauppauge, NY: Nova Science Publishers), pp. 35-65
  37. Oster, H., Damerow, S., Kiessling, S., Jakubcakova, V., Abraham, D., Tian, J., Hoffmann, M.W., and Eichele, G. (2006). The circadian rhythm of glucocorticoids is regulated by a gating mechanism residing in the adrenal cortical clock. Cell Metab. 4,163-173 https://doi.org/10.1016/j.cmet.2006.07.002
  38. Pan, X., and Hussain, M.M. (2009). Clock is important for food and circadian regulation of macronutrient absorption in mice. J. Lipid Res. [Epub ahead of print] https://doi.org/10.1194/jlr.M900085-JLR200
  39. Pittendrigh, C.S. (1993). Temporal organization: reflections of a Darwinian clock-watcher. Annu. Rev. Physiol. 55, 16-54 https://doi.org/10.1146/annurev.ph.55.030193.000313
  40. Preitner, N., Damiola, F., Lopez-Molina, L., Zakany, J., Duboule, D., Albrecht, U., and Schibler, U. (2002). The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110, 251-260 https://doi.org/10.1016/S0092-8674(02)00825-5
  41. 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., et al. (2009). Circadian clock feedback cycle through NAMPTmediated NAD+ biosynthesis. Science 324, 651-654 https://doi.org/10.1126/science.1171641
  42. Raspe, E., Duez, H., Mansen, A., Fontaine, C., Fievet, C., Fruchart, J.-C., Vennstrom, B., and Staels, B. (2002). Identification of Reverb{alpha} as a physiological repressor of apoC-III gene transcription. J. Lipid Res. 43, 2172-2179 https://doi.org/10.1194/jlr.M200386-JLR200
  43. Resnick, H.E., Redline, S., Shahar, E., Gilpin, A., Newman, A., Walter, R., Ewy, G.A., Howard, B.V., and Punjabi, N.M. (2003). Diabetes and sleep disturbances: findings from the Sleep Heart Health Study. Diabetes Care 26, 702-709 https://doi.org/10.2337/diacare.26.3.702
  44. Rudic, R.D., McNamara, P., Curtis, A.M., Boston, R.C., Panda, S., Hogenesch, J.B., and Fitzgerald, G.A. (2004). BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biol. 2, e377 https://doi.org/10.1371/journal.pbio.0020377
  45. Rutter, J., Reick, M., Wu, L.C., and McKnight, S.L. (2001). Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science 293, 510-514 https://doi.org/10.1126/science.1060698
  46. Sato, T.K., Panda, S., Miraglia, L.J., Reyes, T.M., Rudic, R.D., McNamara, P., Naik, K.A., FitzGerald, G.A., Kay, S.A., and Hogenesch, J.B. (2004). A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron 43, 527-537 https://doi.org/10.1016/j.neuron.2004.07.018
  47. Scott, E.M., Carter, A.M., and Grant, P.J. (2007). Association between polymorphisms in the Clock gene, obesity and the metabolic syndrome in man. Int. J. Obes. 32, 658-662 https://doi.org/10.1038/sj.ijo.0803778
  48. Shea, S.A., Hilton, M.F., Orlova, C., Ayers, R.T., and Mantzoros, C.S. (2005). Independent circadian and sleep/wake regulation of adipokines and glucose in humans. J. Clin. Endocrinol. Metab.90, 2537-2544 https://doi.org/10.1210/jc.2004-2232
  49. Shimba, S., Ishii, N., Ohta, Y., Ohno, T., Watabe, Y., Hayashi, M., Wada, T., Aoyagi, T., and Tezuka, M. (2005). Brain and muscle Arnt-like protein-1 (BMAL1), a component of the molecular clock, regulates adipogenesis. Proc. Natl. Acad. Sci. USA 102, 12071-12076 https://doi.org/10.1073/pnas.0502383102
  50. Spanagel, R., Pendyala, G., Abarca, C., Zghoul, T., Sanchis- Segura, C., Magnone, M.C., Lascorz, J., Depner, M., Holzberg, D., Soyka, M.,=et al. (2005). The clock gene Per2 influences the glutamatergic system and modulates alcohol consumption. Nat. Med. 11, 35-42 https://doi.org/10.1038/nm1163
  51. Spiegel, K., Leproult, R., and Van Cauter, E. (1999). Impact of sleep debt on metabolic and endocrine function. Lancet 354, 1435-1439 https://doi.org/10.1016/S0140-6736(99)01376-8
  52. Spiegel, K., Tasali, E., Penev, P., and Cauter, E.V. (2004). Brief communication: sleep curtailment in healthy young men is associated with decreased leptin levels, elevated ghrelin levels, and increased hunger and appetite. Ann. Intern. Med. 141, 846-850 https://doi.org/10.1001/archinte.141.7.846
  53. Stratmann, M., and Schibler, U. (2006). Properties, entrainment, and physiological functions of Mammalian peripheral oscillators. J. Biol. Rhythms 21, 494-506 https://doi.org/10.1177/0748730406293889
  54. Takahashi, J.S., Hong, H.K., Ko, C.H., and McDearmon, E.L. (2008). The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat. Rev. Genet. 9, 764-775 https://doi.org/10.1038/nrg2430
  55. Turek, F.W., Joshu, C., Kohsaka, A., Lin, E., Ivanova, G., McDearmon, E., Laposky, A., Losee-Olson, S., Easton, A., Jensen, D.R., et al. (2005). Obesity and metabolic syndrome in circadian Clock mutant mice. Science 308, 1043-1045 https://doi.org/10.1126/science.1108750
  56. Van Cauter, E., Polonsky, K.S., and Scheen, A.J. (1997). Roles of circadian rhythmicity and sleep in human glucose regulation. Endocr. Rev. 18, 716-738 https://doi.org/10.1210/er.18.5.716
  57. Wang, J., and Lazar, M.A. (2008). Bifunctional role of Rev-erbalpha in adipocyte differentiation. Mol. Cell. Biol. 28, 2213-2220 https://doi.org/10.1128/MCB.01608-07
  58. Wittmann, M., Dinich, J., Merrow, M., and Roenneberg, T. (2006). Social jetlag: misalignment of biological and social time. Chronobiol. Int. 23, 497-509 https://doi.org/10.1080/07420520500545979
  59. Woelfle, M.A., Ouyang, Y., Phanvijhitsiri, K., and Johnson, C.H. (2004). The adaptive value of circadian clocks: an experimental assessment in cyanobacteria. Curr. Biol. 14, 1481-1486 https://doi.org/10.1016/j.cub.2004.08.023
  60. Woon, P.Y., Kaisaki, P.J., Braganca, J., Bihoreau, M.-T., Levy, J.C., Farrall, M., and Gauguier, D. (2007). Aryl hydrocarbon receptor nuclear translocator-like (BMAL1) is associated with susceptibility to hypertension and type 2 diabetes. Proc. Natl. Acad. Sci. USA 104, 14412-14417 https://doi.org/10.1073/pnas.0703247104
  61. Yang, X., Downes, M., Yu, R.T., Bookout, A.L., He, W., Straume, M., Mangelsdorf, D.J., and Evans, R.M. (2006). Nuclear receptor expression links the circadian clock to metabolism. Cell 126, 801-810 https://doi.org/10.1016/j.cell.2006.06.050
  62. Yang, S., Liu, A., Weidenhammer, A., Cooksey, R.C., McClain, D., Kim, M.K., Aguilera, G., Abel, E.D., and Chung, J.H. (2009). The role of mPer2 Clock gene in glucocorticoid and feeding rhythms. Endocrinology 150, 2153-2160 https://doi.org/10.1210/en.2008-0705
  63. Yildiz, B.O., Suchard, M.A., Wong, M.L., McCann, S.M., and Licinio, J. (2004). Alterations in the dynamics of circulating ghrelin, adiponectin, and leptin in human obesity. Proc. Natl. Acad. Sci. USA 101, 10434-10439 https://doi.org/10.1073/pnas.0403465101
  64. 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., et al. (2007). Rev-erbalpha, a heme sensor that coordinates metabolic and circadian pathways. Science 318, 1786-1789 https://doi.org/10.1126/science.1150179

Cited by

  1. THE CROSSTALK BETWEEN PHYSIOLOGY AND CIRCADIAN CLOCK PROTEINS vol.26, pp.8, 2009, https://doi.org/10.3109/07420520903497575
  2. A wheel of time: the circadian clock, nuclear receptors, and physiology: Figure 1. vol.24, pp.8, 2009, https://doi.org/10.1101/gad.1920710
  3. Circadian Control of Global Gene Expression Patterns vol.44, pp.None, 2009, https://doi.org/10.1146/annurev-genet-102209-163432
  4. Deficient of a Clock Gene, Brain and Muscle Arnt-Like Protein-1 (BMAL1), Induces Dyslipidemia and Ectopic Fat Formation vol.6, pp.9, 2011, https://doi.org/10.1371/journal.pone.0025231
  5. Thiol-disulfide Redox Dependence of Heme Binding and Heme Ligand Switching in Nuclear Hormone Receptor Rev-erbβ vol.286, pp.6, 2009, https://doi.org/10.1074/jbc.m110.193466
  6. Understanding systems-level properties: timely stories from the study of clocks vol.12, pp.6, 2009, https://doi.org/10.1038/nrg2972
  7. Hypothalamus integrity and appetite regulation in low birth weight rats reared artificially on a high-protein milk formula vol.22, pp.10, 2009, https://doi.org/10.1016/j.jnutbio.2010.08.007
  8. Differentiated embryo chondrocyte 1 (DEC1) represses PPARγ2 gene through interacting with CCAAT/enhancer binding protein β (C/EBPβ) vol.33, pp.6, 2009, https://doi.org/10.1007/s10059-012-0002-9
  9. R-α-lipoic acid does not reverse hepatic inflammation of aging, but lowers lipid anabolism, while accentuating circadian rhythm transcript profiles vol.302, pp.5, 2009, https://doi.org/10.1152/ajpregu.00393.2011
  10. Expression of circadian gens in different rat tissues is sensitive marker of in vivo silver nanoparticles action vol.40, pp.None, 2012, https://doi.org/10.1088/1757-899x/40/1/012016
  11. Circadian Clock Genes Per1 and Per2 Regulate the Response of Metabolism-Associated Transcripts to Sleep Disruption vol.7, pp.12, 2012, https://doi.org/10.1371/journal.pone.0052983
  12. Timed high-fat diet in the evening affects the hepatic circadian clock and PPARα-mediated lipogenic gene expressions in mice vol.8, pp.5, 2009, https://doi.org/10.1007/s12263-013-0333-y
  13. The Expression of <i>TIMP</i>1, <i>TIMP</i>2, <i>VCAN</i>, <i>SPARC</i>, <i&g vol.2, pp.2, 2009, https://doi.org/10.4236/cellbio.2013.22006
  14. Time-of-day of energy intake: association with hypertension and blood pressure 10 years later in the 1946 British Birth Cohort vol.31, pp.5, 2009, https://doi.org/10.1097/hjh.0b013e32835ecc06
  15. Circadian Rhythm of Energy Expenditure and Oxygen Consumption vol.38, pp.2, 2009, https://doi.org/10.1177/0148607113482331
  16. Crossroads between light response and nutrient signalling: ENV1 and PhLP1 act as mutual regulatory pair in Trichoderma reesei vol.15, pp.1, 2009, https://doi.org/10.1186/1471-2164-15-425
  17. Circadian Misalignment Augments Markers of Insulin Resistance and Inflammation, Independently of Sleep Loss vol.63, pp.6, 2009, https://doi.org/10.2337/db13-1546
  18. Adrenal Clocks and the Role of Adrenal Hormones in the Regulation of Circadian Physiology vol.30, pp.1, 2015, https://doi.org/10.1177/0748730414553971
  19. Comparative Transcriptomic Analyses by RNA-seq to Elucidate Differentially Expressed Genes in the Muscle of Korean Thoroughbred Horses vol.180, pp.3, 2009, https://doi.org/10.1007/s12010-016-2118-4
  20. Microbes at Surface-Air Interfaces: The Metabolic Harnessing of Relative Humidity, Surface Hygroscopicity, and Oligotrophy for Resilience vol.7, pp.None, 2009, https://doi.org/10.3389/fmicb.2016.01563
  21. The Defense Metabolite, Allyl Glucosinolate, Modulates Arabidopsis thaliana Biomass Dependent upon the Endogenous Glucosinolate Pathway vol.7, pp.None, 2009, https://doi.org/10.3389/fpls.2016.00774
  22. Meal Timing and Frequency: Implications for Cardiovascular Disease Prevention: A Scientific Statement From the American Heart Association vol.135, pp.9, 2017, https://doi.org/10.1161/cir.0000000000000476
  23. Molecular Aspects of Circadian Pharmacology and Relevance for Cancer Chronotherapy vol.18, pp.10, 2017, https://doi.org/10.3390/ijms18102168
  24. Repercussions of hypo and hyperthyroidism on the heart circadian clock vol.35, pp.2, 2009, https://doi.org/10.1080/07420528.2017.1388253
  25. An incoherent feed-forward loop switches the Arabidopsis clock rapidly between two hysteretic states vol.8, pp.None, 2009, https://doi.org/10.1038/s41598-018-32030-z
  26. Multilevel Interactions of Stress and Circadian System: Implications for Traumatic Stress vol.10, pp.None, 2009, https://doi.org/10.3389/fpsyt.2019.01003
  27. Interaction Between Circadian Rhythms, Energy Metabolism, and Cognitive Function vol.26, pp.20, 2020, https://doi.org/10.2174/1381612826666200310145006
  28. Basal leakage in oscillation: Coupled transcriptional and translational control using feed-forward loops vol.16, pp.9, 2009, https://doi.org/10.1371/journal.pcbi.1007740