The role of the circadian timing system on drug metabolism and detoxification: an update

References

• Pittendrigh CS. Temporal organization: reflections of a Darwinian clock-watcher. Annu Rev Physiol. 1993;55(1):17–54. doi: 10.1146/annurev.ph.55.030193.000313
   Google Scholar
• Kavakli IH, Sancar A Circadian photoreception in humans and mice. Mol Interv. 2002;2:484–492. 8 10.1124/mi.2.8.484
   PubMedGoogle Scholar
• Dibner C, Schibler U, Albrecht U. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol. 2010;72(1):517–549. doi: 10.1146/annurev-physiol-021909-135821
   PubMed Web of Science ®Google Scholar
• Ralph MR, Foster RG, Davis FC, et al. Transplanted suprachiasmatic nucleus determines circadian period. Science. 1990;247(4945):975–978. doi: 10.1126/science.2305266
   PubMed Web of Science ®Google Scholar
• Mohawk JA, Green CB, Takahashi JS. Central and peripheral circadian clocks in mammals. Annu Rev Neurosci. 2012;35(1):445–462. doi: 10.1146/annurev-neuro-060909-153128
   PubMed Web of Science ®Google Scholar
• Hara R, Wan K, Wakamatsu H, et al. Restricted feeding entrains liver clock without participation of the suprachiasmatic nucleus. Genes Cells. 2001;6(3):269–278. doi: 10.1046/j.1365-2443.2001.00419.x
   PubMed Web of Science ®Google Scholar
• Kohsaka A, Laposky AD, Ramsey KM, et al. High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab. 2007;6(5):414–421. doi: 10.1016/j.cmet.2007.09.006
   PubMed Web of Science ®Google Scholar
• Asher G, Gatfield D, Stratmann M, et al. SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell. 2008;134(2):317–328. doi: 10.1016/j.cell.2008.06.050
   PubMed Web of Science ®Google Scholar
• López-Otín C, Galluzzi L, Freije JMP, et al. Metabolic control of longevity. Cell. 2016;166(4):802–821. doi: 10.1016/j.cell.2016.07.031
   PubMed Web of Science ®Google Scholar
• Astiz M, Heyde I, Oster H. Mechanisms of communication in the Mammalian Circadian Timing System. Int J Mol Sci. 2019;20(2):343. doi: 10.3390/ijms20020343
   PubMed Web of Science ®Google Scholar
• Nedeltcheva AV, Scheer FAJL. Metabolic effects of sleep disruption, links to obesity and diabetes. Curr Opin Endocrinol Diabetes Obes. 2014;21:293–298.10.1097/MED.0000000000000082
   PubMed Web of Science ®Google Scholar
• Parsons MJ, Moffitt TE, Gregory AM, et al. Social jetlag, obesity and metabolic disorder: investigation in a cohort study. Int J Obes (Lond). 2015;39(5):842–848. doi: 10.1038/ijo.2014.201
   PubMed Web of Science ®Google Scholar
• Baris I, Ozcan O, Kavakli IH Single nucleotide polymorphisms (SNPs) in circadian genes: Impact on gene function and phenotype. Adv Protein Chem Struct Biol. 2023;137:17–37.
   PubMedGoogle Scholar
• Clench J, Reinberg A, Dziewanowska Z, et al. Circadian changes in the bioavailability and effects of indomethacin in healthy subjects. Eur J Clin Pharmacol. 1981;20(5):359–369. doi: 10.1007/BF00615406
   PubMed Web of Science ®Google Scholar
• Reinberg A. New aspects of human chronopharmacology. Arch Toxicol. 1976;36(3–4):327–339. doi: 10.1007/BF00340538
   PubMed Web of Science ®Google Scholar
• Reinberg A, Halberg F. Circadian chronopharmacology. Ann Rev Pharmacol. 1971;11(1):455–492. doi: 10.1146/annurev.pa.11.040171.002323
   PubMedGoogle Scholar
• Levi F, Schibler U. Circadian rhythms: mechanisms and therapeutic implications. Annu Rev Pharmacol Toxicol. 2007;47(1):593–628. doi: 10.1146/annurev.pharmtox.47.120505.105208
   PubMedGoogle Scholar
• Nahmias Y, Androulakis IP Circadian Effects of Drug Responses. Annu Rev Biomed Eng. 2021;23:203–224. 1 10.1146/annurev-bioeng-082120-034725
   PubMedGoogle Scholar
• Lévi FA, Okyar A, Hadadi E, et al. Circadian Regulation of Drug Responses: Toward Sex-Specific and Personalized Chronotherapy. Annu Rev Pharmacol Toxicol. 2024;64:89–114. 1 10.1146/annurev-pharmtox-051920-095416
   PubMedGoogle Scholar
• Kavakli IH, Baris I, Tardu M, et al. The Photolyase/Cryptochrome Family of Proteins as DNA Repair Enzymes and Transcriptional Repressors. Photochem Photobio. 2017;93(1):93–103. doi: 10.1111/php.12669
   PubMed Web of Science ®Google Scholar
• Takahashi JS. Transcriptional architecture of the mammalian circadian clock. Nat Rev Genet. 2017;18(3):164–179. doi: 10.1038/nrg.2016.150
   PubMed Web of Science ®Google Scholar
• Allada R, Bass J, Longo DL Circadian Mechanisms in Medicine. Longo DL, editor. N Engl J Med. 2021;384:550–561. 6 10.1056/NEJMra1802337
   PubMed Web of Science ®Google Scholar
• Kavakli IH, Gul S, Turkay M. Identification of novel small molecules targeting core clock proteins to regulate circadian rhythm. Curr Opin Chem Eng. 2022;35:100730.
   Web of Science ®Google Scholar
• Sancar A. Cryptochrome: the second photoactive pigment in the eye and its role in circadian photoreception. Annu Rev Biochem. 2000;69:31–67. 1 10.1146/annurev.biochem.69.1.31
   PubMedGoogle Scholar
• Cox KH, Takahashi JS. Circadian clock genes and the transcriptional architecture of the clock mechanism. J Mol Endocrinol. 2019;63(4):R93–R102. doi: 10.1530/JME-19-0153
   PubMed Web of Science ®Google Scholar
• Gallego M, Virshup DM. Post-translational modifications regulate the ticking of the circadian clock. Nat Rev Mol Cell Biol. 2007;8(2):139–148. doi: 10.1038/nrm2106
   PubMed Web of Science ®Google Scholar
• Meng Q-J, Logunova L, Maywood ES, et al. Setting Clock Speed in Mammals: The CK1ɛ tau Mutation in Mice Accelerates Circadian Pacemakers by Selectively Destabilizing PERIOD Proteins. Neuron. 2008;58:78–88. 1 10.1016/j.neuron.2008.01.019
   PubMed Web of Science ®Google Scholar
• Lee Y. Roles of circadian clocks in cancer pathogenesis and treatment. Exp Mol Med. 2021;53(10):1529–1538. doi: 10.1038/s12276-021-00681-0
   PubMed Web of Science ®Google Scholar
• Ueda HR, Hayashi S, Chen W, et al. System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat Genet. 2005;37(2):187–192. doi: 10.1038/ng1504
   PubMed Web of Science ®Google Scholar
• Yamaguchi S, Mitsui S, Yan L, et al. Role of DBP in the circadian oscillatory mechanism. Mol Cell Biol. 2000;20(13):4773–4781. doi: 10.1128/MCB.20.13.4773-4781.2000
   PubMed Web of Science ®Google Scholar
• Mitsui S, Yamaguchi S, Matsuo T, et al. Antagonistic role of E4BP4 and PAR proteins in the circadian oscillatory mechanism. Genes Dev. 2001;15(8):995–1006. doi: 10.1101/gad.873501
   PubMed Web of Science ®Google Scholar
• Gachon F, Fonjallaz P, Damiola F, et al. The loss of circadian PAR bZip transcription factors results in epilepsy. Genes Dev. 2004;18(12):1397–1412. doi: 10.1101/gad.301404
   PubMed Web of Science ®Google Scholar
• Weger BD, Gobet C, David FPA, et al. Systematic analysis of differential rhythmic liver gene expression mediated by the circadian clock and feeding rhythms. Proc Natl Acad Sci U S A. 2021;118(3):e2015803118. doi: 10.1073/pnas.2015803118
   PubMed Web of Science ®Google Scholar
• Yoshitane H, Asano Y, Sagami A, et al. Functional D-box sequences reset the circadian clock and drive mRNA rhythms. Commun Biol. 2019;2(1):300. doi: 10.1038/s42003-019-0522-3
   PubMedGoogle Scholar
• Cowell IG. E4BP4/NFIL3, a PAR-related bZIP factor with many roles. BioEssays. 2002;24(11):1023–1029. doi: 10.1002/bies.10176
   PubMed Web of Science ®Google Scholar
• Junghans D, Chauvet S, Buhler E, et al. The CES-2-related transcription factor E4BP4 is an intrinsic regulator of motoneuron growth and survival. Development. 2004;131(18):4425–4434. doi: 10.1242/dev.01313
   PubMed Web of Science ®Google Scholar
• Silvestris F, Cafforio P, De Matteo M, et al. Negative regulation of the osteoblast function in multiple myeloma through the repressor gene E4BP4 activated by malignant plasma cells. Clin Cancer Res. 2008;14(19):6081–6091. doi: 10.1158/1078-0432.CCR-08-0219
   PubMed Web of Science ®Google Scholar
• Zhao M, Wang Y, Chen M, et al. Introduction to Pharmacokinetics. In: Wu B, Lu D Dong D, editors Circadian Pharmacokinetics [Internet]. Singapore: Springer Singapore; 2020 [cited 2023 Oct 31]. p. 23–40. Available from: https://doi.org/10.1007/978-981-15-8807-5_2
   Google Scholar
• Akyel YK, Ozturk Civelek D, Ozturk Seyhan N, et al. Diurnal Changes in Capecitabine Clock-Controlled Metabolism Enzymes Are Responsible for Its Pharmacokinetics in Male Mice. J Biol Rhythms. 2023;38(2):171–184. doi: 10.1177/07487304221148779
   PubMed Web of Science ®Google Scholar
• Zhang Y-K, Yeager RL, Klaassen CD Circadian Expression Profiles of Drug-Processing Genes and Transcription Factors in Mouse Liver. Drug Metab Dispos. 2009;37:106–115. 1 10.1124/dmd.108.024174
   PubMed Web of Science ®Google Scholar
• Chen X, Yu F, Guo X, et al. Clock gene Bmal1 controls diurnal rhythms in expression and activity of intestinal carboxylesterase 1. J Pharm Pharmacol. 2021;73(1):52–59. doi: 10.1093/jpp/rgaa035
   PubMed Web of Science ®Google Scholar
• Lee Y, Shen Y, Francey LJ, et al. The NRON complex controls circadian clock function through regulated per and CRY nuclear translocation. Sci Rep. 2019;9(1):11883. doi: 10.1038/s41598-019-48341-8
   PubMedGoogle Scholar
• Anafi RC, Lee Y, Sato TK, et al. Machine Learning Helps Identify CHRONO as a Circadian Clock Component. PLoS Biol. 2014;12(4):e1001840. doi: 10.1371/journal.pbio.1001840
   PubMed Web of Science ®Google Scholar
• Cal-Kayitmazbatir S, Kulkoyluoglu-Cotul E, Growe J, et al. CRY1-CBS binding regulates circadian clock function and metabolism. FEBS J. 2021;288(2):614–639. doi: 10.1111/febs.15360
   PubMed Web of Science ®Google Scholar
• Ozturk N, Ozturk D, Kavakli IH, et al. Molecular Aspects of Circadian Pharmacology and Relevance for Cancer Chronotherapy. IJMS. 2017;18(10):2168. doi: 10.3390/ijms18102168
   Google Scholar
• Zhang T, Yu F, Guo L, et al. Circadian Clock and CYP Metabolism. In: Wu B, Lu D Dong D, editors Circadian Pharmacokinetics [Internet]. Singapore: Springer Singapore; 2020 [cited 2023 Oct 31]. p. 65–87. Available from: https://doi.org/10.1007/978-981-15-8807-5_4
   Google Scholar
• Lu Y-F, Jin T, Xu Y, et al. Sex Differences in the Circadian Variation of Cytochrome P450 Genes and Corresponding Nuclear Receptors in Mouse Liver. Chronobiol Int. 2013;30(9):1135–1143. doi: 10.3109/07420528.2013.805762
   PubMed Web of Science ®Google Scholar
• Weger M, Weger BD, Gachon F. Understanding circadian dynamics: current progress and future directions for chronobiology in drug discovery. Expert Opin Drug Discov. 2023;18(8):893–901. doi: 10.1080/17460441.2023.2224554
   PubMed Web of Science ®Google Scholar
• Gachon F, Olela FF, Schaad O, et al. The circadian PAR-domain basic leucine zipper transcription factors DBP, TEF, and HLF modulate basal and inducible xenobiotic detoxification. Cell Metab. 2006;4(1):25–36. doi: 10.1016/j.cmet.2006.04.015
   PubMed Web of Science ®Google Scholar
• Chen M, Zhou C, Zhang T, et al. Identification of rhythmic human CYPs and their circadian regulators using synchronized hepatoma cells. Xenobiotica. 2020;50(9):1052–1063. doi: 10.1080/00498254.2020.1737890
   PubMed Web of Science ®Google Scholar
• Li H, Zhang S, Zhang W, et al. Endogenous circadian time genes expressions in the liver of mice under constant darkness. BMC Genomics. 2020;21(1):224. doi: 10.1186/s12864-020-6639-4
   PubMed Web of Science ®Google Scholar
• Zhao M, Zhao H, Deng J, et al. Role of the CLOCK protein in liver detoxification. Br J Pharmacol. 2019;176(24):4639. doi: 10.1111/bph.14828
   PubMed Web of Science ®Google Scholar
• He Y, Cen H, Guo L, et al. Circadian oscillator NPAS2 regulates diurnal expression and activity of CYP1A2 in mouse liver. Biochem Pharmacol. 2022;206:115345.10.1016/j.bcp.2022.115345
   PubMed Web of Science ®Google Scholar
• Lin Y, Wang S, Zhou Z, et al. Bmal1 regulates circadian expression of cytochrome P450 3a11 and drug metabolism in mice. Commun Biol. 2019;2(1):378. doi: 10.1038/s42003-019-0607-z
   PubMedGoogle Scholar
• Tong Y, Zeng P, Zhang T, et al. The transcription factor E4bp4 regulates the expression and activity of Cyp3a11 in mice. Biochem Pharmacol. 2019;163:215–224.10.1016/j.bcp.2019.02.026
   PubMed Web of Science ®Google Scholar
• Lin L, Huang Y, Wang J, et al. CRY1/2 regulate rhythmic CYP2A5 in mouse liver through repression of E4BP4. Biochem Pharmacol. 2023;217:115843.10.1016/j.bcp.2023.115843
   PubMed Web of Science ®Google Scholar
• Deng J, Guo L, Wu B. Circadian Regulation of Hepatic Cytochrome P450 2a5 by peroxisome proliferator-activated receptor γ. Drug Metab Dispos. 2018;46(11):1538–1545. doi: 10.1124/dmd.118.083071
   PubMed Web of Science ®Google Scholar
• Sundekilde UK, Kristensen CM, Olsen MA, et al. Time-dependent regulation of hepatic cytochrome P450 mRNA in male liver-specific PGC-1α knockout mice. Toxicology. 2022;469:153121.10.1016/j.tox.2022.153121
   PubMed Web of Science ®Google Scholar
• Poliandri AHB, Gamsby JJ, Christian M, et al. Modulation of Clock Gene Expression by the Transcriptional Coregulator Receptor Interacting Protein 140 (RIP140). J Biol Rhythms. 2011;26(3):187–199. doi: 10.1177/0748730411401579
   PubMed Web of Science ®Google Scholar
• Zhao M, Zhao H, Lin L, et al. Nuclear receptor co-repressor RIP140 regulates diurnal expression of cytochrome P450 2b10 in mouse liver. Xenobiotica. 2020;50(10):1139–1148. doi: 10.1080/00498254.2020.1751342
   PubMed Web of Science ®Google Scholar
• Wu N, Kim KH, Zhou Y, et al. Small heterodimer partner (NR0B2) coordinates nutrient signaling and the circadian clock in mice. Mol Endocrinol. 2016;30(9):988–995. doi: 10.1210/me.2015-1295
   PubMedGoogle Scholar
• Zhang T, Yu F, Guo L, et al. Small Heterodimer Partner Regulates Circadian Cytochromes p450 and Drug-Induced Hepatotoxicity. Theranostics. 2018;8(19):5246–5258. doi: 10.7150/thno.28676
   PubMed Web of Science ®Google Scholar
• Hwang D-B, Won D-H, Shin Y-S, et al. Ccrn4l as a pre-dose marker for prediction of cisplatin-induced hepatotoxicity susceptibility. Free Radic Biol Med. 2020;148:128–139.10.1016/j.freeradbiomed.2020.01.003
   PubMed Web of Science ®Google Scholar
• Lu J, Wang H, Zhang R, et al. Effects of photoperiod on acetaminophen-induced hepatotoxicity in mice. Dig Dis Sci. 2020;65(1):178–188. doi: 10.1007/s10620-019-05749-6
   PubMed Web of Science ®Google Scholar
• Ge W, Wang T, Zhao Y, et al. Period1 mediates rhythmic metabolism of toxins by interacting with CYP2E1. Cell Death Dis. 2021;12(1):76. doi: 10.1038/s41419-020-03343-7
   PubMed Web of Science ®Google Scholar
• Wang L, Liu Y, Gao H, et al. Chronotoxicity of Acrylamide in Mice Fed a High-Fat Diet: The Involvement of Liver CYP2E1 Upregulation and Gut Leakage. Molecules. 2023;28(13):5132. doi: 10.3390/molecules28135132
   PubMed Web of Science ®Google Scholar
• Gängler S, Charisiadis P, Seth R, et al. Time of the day dictates the variability of biomarkers of exposure to disinfection byproducts. Environ Int. 2018;112:33–40. 10.1016/j.envint.2017.12.013
   PubMed Web of Science ®Google Scholar
• Guo L, Zhang L, Xu H, et al. Diurnal hepatic CYP3A11 contributes to chronotoxicity of the pyrrolizidine alkaloid retrorsine in mice. Xenobiotica. 2021;51(9):1019–1028. doi: 10.1080/00498254.2021.1950867
   PubMed Web of Science ®Google Scholar
• Zhao H, Tong Y, Lu D, et al. Circadian clock regulates hepatotoxicity of tripterygium wilfordii through modulation of metabolism. J Pharm Pharmacol. 2020;72(12):1854–1864. doi: 10.1111/jphp.13299
   PubMed Web of Science ®Google Scholar
• Zhou Z, Lin Y, Gao L, et al. Cyp3a11 metabolism-based chronotoxicity of brucine in mice. Toxicol Lett. 2019;313:188–195. 10.1016/j.toxlet.2019.07.007
   PubMed Web of Science ®Google Scholar
• Lin Y, Zhou Z, Yang Z, et al. Circadian Cyp3a11 metabolism contributes to chronotoxicity of hypaconitine in mice. Chem Biol Interact. 2019;308:288–293.10.1016/j.cbi.2019.05.049
   PubMed Web of Science ®Google Scholar
• Zhao M, Zhang T, Yu F, et al. E4bp4 regulates carboxylesterase 2 enzymes through repression of the nuclear receptor Rev-erbα in mice. Biochem Pharmacol. 2018;152:293–301.10.1016/j.bcp.2018.04.005
   PubMed Web of Science ®Google Scholar
• Zhu H-J, Wang X, Gawronski BE, et al. Carboxylesterase 1 as a determinant of clopidogrel metabolism and activation. J Pharmacol Exp Ther. 2013;344(3):665–672. doi: 10.1124/jpet.112.201640
   PubMed Web of Science ®Google Scholar
• Ma L, Yu F, He D, et al. Role of circadian clock in the chronoefficacy and chronotoxicity of clopidogrel. Br J Pharmacol.2023;180. 23 2973–2988 10.1111/bph.16188
   PubMed Web of Science ®Google Scholar
• Yu F, Liu Y, Zhang R, et al. Recent advances in circadian-regulated pharmacokinetics and its implications for chronotherapy. Biochem Pharmacol. 2022;203:115185. 10.1016/j.bcp.2022.115185
   PubMed Web of Science ®Google Scholar
• Zhang T, Guo L, Yu F, et al. The nuclear receptor Rev-erbα participates in circadian regulation of Ugt2b enzymes in mice. Biochem Pharmacol. 2019 [cited 2023 Oct 31];161:89–97. doi: 10.1016/j.bcp.2019.01.010
   PubMed Web of Science ®Google Scholar
• Xu H, Chen M, Yu F, et al. Circadian Clock Component Rev-erbα Regulates Diurnal Rhythm of UDP-Glucuronosyltransferase 1a9 and drug glucuronidation in mice. Drug Metab Dispos. 2020;48(8):681–689. doi: 10.1124/dmd.120.000030
   PubMed Web of Science ®Google Scholar
• Guo L, Yu F, Zhang T, et al. The Clock Protein Bmal1 Regulates Circadian Expression and activity of sulfotransferase 1a1 in mice. Drug Metab Dispos. 2018;46(10):1403–1410. doi: 10.1124/dmd.118.082503
   PubMed Web of Science ®Google Scholar
• Lévi F, Okyar A, Dulong S, et al. Circadian timing in cancer treatments. Annu Rev Pharmacol Toxicol. 2010;50(1):377–421. doi: 10.1146/annurev.pharmtox.48.113006.094626
   PubMed Web of Science ®Google Scholar
• Houghton SG, Zarroug AE, Duenes JA, et al. The diurnal periodicity of hexose transporter mRNA and protein levels in the rat jejunum: role of vagal innervation. Surgery. 2006;139(4):542–549. doi: 10.1016/j.surg.2005.09.002
   PubMed Web of Science ®Google Scholar
• Iwashina I, Mochizuki K, Inamochi Y, et al. Clock genes regulate the feeding schedule-dependent diurnal rhythm changes in hexose transporter gene expressions through the binding of BMAL1 to the promoter/enhancer and transcribed regions. J Nutr Biochem. 2011;22(4):334–343. doi: 10.1016/j.jnutbio.2010.02.012
   PubMed Web of Science ®Google Scholar
• Stearns AT, Balakrishnan A, Rhoads DB, et al. Diurnal rhythmicity in the transcription of jejunal drug transporters. J Pharmacol Sci. 2008;108(1):144–148. doi: 10.1254/jphs.08100SC
   PubMed Web of Science ®Google Scholar
• Vagnerová K, Ergang P, Soták M, et al. Diurnal expression of ABC and SLC transporters in jejunum is modulated by adrenalectomy. Comp Biochem Physiol C Toxicol Pharmacol. 2019;226:108607. 10.1016/j.cbpc.2019.108607
   PubMed Web of Science ®Google Scholar
• Tsurudome Y, Koyanagi S, Kanemitsu T, et al. Circadian clock component PERIOD2 regulates diurnal expression of Na+/H+ exchanger regulatory factor-1 and its scaffolding function. Sci Rep. 2018;8(1):9072. doi: 10.1038/s41598-018-27280-w
   PubMedGoogle Scholar
• Miyagawa A, Tatsumi S, Takahama W, et al. The sodium phosphate cotransporter family and nicotinamide phosphoribosyltransferase contribute to the daily oscillation of plasma inorganic phosphate concentration. Kidney Int. 2018;93(5):1073–1085. doi: 10.1016/j.kint.2017.11.022
   PubMed Web of Science ®Google Scholar
• Nikolaeva S, Ansermet C, Centeno G, et al. Nephron-specific deletion of circadian clock gene Bmal1 alters the plasma and renal metabolome and impairs drug disposition. J Am Soc Nephrol. 2016;27(10):2997–3004. doi: 10.1681/ASN.2015091055
   PubMed Web of Science ®Google Scholar
• Oh J-H, Lee JH, Han D-H, et al. Circadian Clock Is Involved in Regulation of hepatobiliary transport mediated by multidrug resistance-associated protein 2. J Pharm Sci. 2017;106(9):2491–2498. doi: 10.1016/j.xphs.2017.04.071
   PubMed Web of Science ®Google Scholar
• Wada E, Koyanagi S, Kusunose N, et al. Modulation of peroxisome proliferator-activated receptor-α activity by bile acids causes circadian changes in the intestinal expression of Octn1/Slc22a4 in mice. Mol Pharmacol. 2015;87(2):314–322. doi: 10.1124/mol.114.094979
   PubMed Web of Science ®Google Scholar
• Okamura A, Koyanagi S, Dilxiat A, et al. Bile acid-regulated peroxisome proliferator-activated receptor-α (PPARα) activity underlies circadian expression of intestinal peptide absorption transporter PepT1/Slc15a1. J Biol Chem. 2014;289(36):25296–25305. doi: 10.1074/jbc.M114.577023
   PubMed Web of Science ®Google Scholar
• Pan X, Terada T, Irie M, et al. Diurnal rhythm of H + -peptide cotransporter in rat small intestine. Am J Physiol Gastrointest Liver Physiol. 2002;283:G57–64. 1 10.1152/ajpgi.00545.2001
   PubMed Web of Science ®Google Scholar
• Balakrishnan A, Stearns A, Rounds J, et al. Diurnal rhythmicity in glucose uptake is mediated by temporal periodicity in the expression of the sodium-glucose co-transporter (SGLT1). Surgery. 2008;143:813–818. 6 10.1016/j.surg.2008.03.018
   PubMed Web of Science ®Google Scholar
• Henriksson E, Huber A-L, Soto EK, et al. The Liver Circadian Clock Modulates Biochemical and Physiological Responses to Metformin. J Biol Rhythms. 2017;32(4):345–358. doi: 10.1177/0748730417710348
   PubMed Web of Science ®Google Scholar
• Oda M, Koyanagi S, Tsurudome Y, et al. Renal circadian clock regulates the dosing-time dependency of cisplatin-induced nephrotoxicity in mice. Mol Pharmacol. 2014;85(5):715–722. doi: 10.1124/mol.113.089805
   PubMed Web of Science ®Google Scholar
• Weger BD, Gobet C, Yeung J, et al. The mouse microbiome is required for sex-specific diurnal rhythms of gene expression and metabolism. Cell Metab. 2019;29(2):362–382.e8. doi: 10.1016/j.cmet.2018.09.023
   PubMed Web of Science ®Google Scholar
• Wang S, Lin Y, Zhou Z, et al. Circadian Clock Gene Bmal1 Regulates Bilirubin Detoxification: A Potential Mechanism of Feedback Control of Hyperbilirubinemia. Theranostics. 2019;9(18):5122–5133. doi: 10.7150/thno.35773
   PubMed Web of Science ®Google Scholar
• Pácha J, Balounová K, Soták M. Circadian regulation of transporter expression and implications for drug disposition. Expert Opin Drug Metab Toxicol. 2021;17(4):425–439. doi: 10.1080/17425255.2021.1868438
   PubMed Web of Science ®Google Scholar
• Dakup PP, Porter KI, Little AA, et al. The circadian clock regulates cisplatin-induced toxicity and tumor regression in melanoma mouse and human models. Oncotarget. 2018;9(18):14524–14538. doi: 10.18632/oncotarget.24539
   PubMedGoogle Scholar
• Omata Y, Yamauchi T, Tsuruta A, et al. RNA editing enzyme ADAR1 governs the circadian expression of P-glycoprotein in human renal cells by regulating alternative splicing of the ABCB1 gene. J Biol Chem. 2021;296:100601. 10.1016/j.jbc.2021.100601
   PubMed Web of Science ®Google Scholar
• Ando H, Yanagihara H, Sugimoto K, et al. Daily rhythms of P-glycoprotein expression in mice. Chronobiol Int. 2005;22(4):655–665. doi: 10.1080/07420520500180231
   PubMed Web of Science ®Google Scholar
• Yu F, Zhang T, Zhou C, et al. The Circadian Clock Gene Bmal1 Controls Intestinal Exporter MRP2 and Drug Disposition. Theranostics. 2019;9(10):2754–2767. doi: 10.7150/thno.33395
   PubMed Web of Science ®Google Scholar
• Kotaka M, Onishi Y, Ohno T, et al. Identification of negative transcriptional factor E4BP4-binding site in the mouse circadian-regulated gene Mdr2. Neurosci Res. 2008;60(3):307–313. doi: 10.1016/j.neures.2007.11.014
   PubMed Web of Science ®Google Scholar
• Kato M, Tsurudome Y, Kanemitsu T, et al. Diurnal expression of MRP4 in bone marrow cells underlies the dosing-time dependent changes in the oxaliplatin-induced myelotoxicity. Sci Rep. 2020;10(1):13484. doi: 10.1038/s41598-020-70321-6
   PubMed Web of Science ®Google Scholar
• Soták M, Polidarová L, Musílková J, et al. Circadian regulation of electrolyte absorption in the rat colon. Am J Physiol Gastrointest Liver Physiol. 2011;301:G1066–G1074. 6 10.1152/ajpgi.00256.2011
   PubMed Web of Science ®Google Scholar
• Hibma JE, Zur AA, Castro RA, et al. The effect of Famotidine, a MATE1-selective inhibitor, on the pharmacokinetics and pharmacodynamics of metformin. Clin Pharmacokinet. 2016;55(6):711–721. doi: 10.1007/s40262-015-0346-3
   PubMed Web of Science ®Google Scholar
• Koike N, Yoo S-H, Huang H-C, et al. Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science. 2012;338(6105):349–354. doi: 10.1126/science.1226339
   PubMed Web of Science ®Google Scholar
• Zhang Y, Guo G, Klaassen CD, et al. Diurnal variations of mouse plasma and hepatic bile acid concentrations as well as expression of biosynthetic enzymes and transporters. PLoS One. 2011;6(2):e16683. doi: 10.1371/journal.pone.0016683
   PubMed Web of Science ®Google Scholar
• Ma K, Xiao R, Tseng H-T, et al. Circadian dysregulation disrupts bile acid homeostasis. PLoS One. 2009;4(8):e6843. doi: 10.1371/journal.pone.0006843
   PubMed Web of Science ®Google Scholar
• Zhang T, Zhao M, Lu D, et al. REV-ERBα regulates CYP7A1 through repression of liver receptor homolog-1. Drug Metab Dispos. 2018;46(3):248–258. doi: 10.1124/dmd.117.078105
   PubMed Web of Science ®Google Scholar
• Okyar A, Kumar SA, Filipski E, et al. Sex-, feeding-, and circadian time-dependency of P-glycoprotein expression and activity - implications for mechanistic pharmacokinetics modeling. Sci Rep. 2019;9(1):10505. doi: 10.1038/s41598-019-46977-0
   PubMedGoogle Scholar
• Murakami Y, Higashi Y, Matsunaga N, et al. Circadian clock-controlled intestinal expression of the multidrug-resistance gene mdr1a in mice. Gastroenterology. 2008;135:1636–1644.e3. 5 10.1053/j.gastro.2008.07.073
   PubMed Web of Science ®Google Scholar
• Okyar A, Piccolo E, Ahowesso C, et al. Strain- and sex-dependent circadian changes in abcc2 transporter expression: implications for irinotecan chronotolerance in mouse ileum. PLoS One. 2011;6(6):e20393. doi: 10.1371/journal.pone.0020393
   PubMed Web of Science ®Google Scholar
• Hamdan AM, Koyanagi S, Wada E, et al. Intestinal expression of mouse Abcg2/breast cancer resistance protein (BCRP) gene is under control of circadian clock-activating transcription factor-4 pathway. J Biol Chem. 2012;287(21):17224–17231. doi: 10.1074/jbc.M111.333377
   PubMed Web of Science ®Google Scholar
• Zhou C, Yu F, Zeng P, et al. Circadian sensitivity to the cardiac glycoside oleandrin is associated with diurnal intestinal P-glycoprotein expression. Biochem Pharmacol. 2019;169:113622. 10.1016/j.bcp.2019.08.024
   PubMed Web of Science ®Google Scholar
• Pan X, Hussain MM. Clock is important for food and circadian regulation of macronutrient absorption in mice. J Lipid Res. 2009;50(9):1800–1813. doi: 10.1194/jlr.M900085-JLR200
   PubMed Web of Science ®Google Scholar
• Saito H, Terada T, Shimakura J, et al. Regulatory mechanism governing the diurnal rhythm of intestinal H+/peptide cotransporter 1 (PEPT1). Am J Physiol Gastrointest Liver Physiol. 2008;295(2):G395–402. doi: 10.1152/ajpgi.90317.2008
   PubMed Web of Science ®Google Scholar
• Ogata S, Ito S, Masuda T, et al. Diurnal Changes in Protein Expression at the Blood–Brain Barrier in Mice. Biol Pharm Bull. 2022;45:751–756. 6 10.1248/bpb.b22-00016
   PubMed Web of Science ®Google Scholar
• Cuddapah VA, Zhang SL, Sehgal A Regulation of the Blood-Brain Barrier by Circadian Rhythms and Sleep. Trends Neurosci. 2019;42:500–510. 10.1016/j.tins.2019.05.001
   PubMed Web of Science ®Google Scholar
• Savolainen H, Meerlo P, Elsinga PH, et al. P-glycoprotein function in the rodent brain displays a daily rhythm, a quantitative in vivo PET study. Aaps J. 2016;18(6):1524–1531. doi: 10.1208/s12248-016-9973-3
   PubMed Web of Science ®Google Scholar
• Kervezee L, Hartman R, van den Berg D-J, et al. Diurnal variation in P-glycoprotein-mediated transport and cerebrospinal fluid turnover in the brain. Aaps J. 2014;16(5):1029–1037. doi: 10.1208/s12248-014-9625-4
   PubMed Web of Science ®Google Scholar
• Zhang SL, Yue Z, Arnold DM, et al. A Circadian Clock in the blood-brain barrier regulates Xenobiotic Efflux. Cell. 2018;173(1):130–139.e10. doi: 10.1016/j.cell.2018.02.017
   PubMed Web of Science ®Google Scholar
• Zhang SL, Lahens NF, Yue Z, et al. A circadian clock regulates efflux by the blood-brain barrier in mice and human cells. Nat Commun. 2021;12(1):617. doi: 10.1038/s41467-020-20795-9
   PubMed Web of Science ®Google Scholar
• Furtado A, Mineiro R, Duarte AC, et al. The daily expression of ABCC4 at the BCSFB affects the transport of its substrate methotrexate. Int J Mol Sci. 2022;23(5):2443. doi: 10.3390/ijms23052443
   PubMed Web of Science ®Google Scholar
• Dulong S, Ballesta A, Okyar A, et al.Identification of Circadian Determinants of Cancer Chronotherapy through in vitro Chronopharmacology and Mathematical Modeling. Mol Cancer Ther. 2015;14:2154–2164. 9 10.1158/1535-7163.MCT-15-0129
   PubMed Web of Science ®Google Scholar
• Ruben MD, Smith DF, FitzGerald GA, et al. Dosing time matters. Science. 2019;365(6453):547–549. doi: 10.1126/science.aax7621
   PubMed Web of Science ®Google Scholar
• Dulong S, de Souza LEB, Machowiak J, et al. Sex and Circadian Timing Modulate Oxaliplatin Hematological and Hematopoietic Toxicities. Pharmaceutics. 2022;14(11):2465. doi: 10.3390/pharmaceutics14112465
   PubMed Web of Science ®Google Scholar
• Talamanca L, Gobet C, Naef F Sex-dimorphic and age-dependent organization of 24-hour gene expression rhythms in humans. Science. 2023;379:478–483. 10.1126/science.add0846 6631
   PubMed Web of Science ®Google Scholar