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Xenobiotica
the fate of foreign compounds in biological systems
Volume 50, 2020 - Issue 5
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Topics in Xenobiochemistry

Circadian clock-controlled drug metabolism and transport

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Pages 495-505 | Received 07 Aug 2019, Accepted 21 Sep 2019, Published online: 01 Oct 2019

References

  • Almon RR, Yang E, Lai W, et al. (2008). Circadian variations in rat liver gene expression: relationships to drug actions. J Pharmacol Exp Ther 326:700–16.
  • Ando H, Yanagihara H, Sugimoto K, et al. (2005). Daily rhythms of P-glycoprotein expression in mice. Chronobiol Int 22:655–65.
  • Bass J, Takahashi JS. (2010). Circadian integration of metabolism and energetics. Science 330:1349–54.
  • Boughattas NA, Levi F, Fournier C, et al. (1990). Stable circadian mechanisms of toxicity of two platinum analogs (cisplatin and carboplatin) despite repeated dosages in mice. J Pharmacol Exp Ther 255:672–9.
  • Brown SA, Zumbrunn G, Fleury-Olela F, et al. (2002). Rhythms of mammalian body temperature can sustain peripheral circadian clocks. Curr Biol 12:1574–83.
  • Bruguerolle B. (1998). Chronopharmacokinetics. Current status. Clin Pharmacokinet 35:83–94.
  • Buhr ED, Yoo SH, Takahashi JS. (2010). Temperature as a universal resetting cue for mammalian circadian oscillators. Science 330:379–85.
  • Cao QR, Kim TW, Choi JS, et al. (2005). Circadian variations in the pharmacokinetics, tissue distribution and urinary excretion of nifedipine after a single oral administration to rats. Biopharm Drug Dispos 26:427–37.
  • Châteauvert N, Côté H. (1998). Circadian variations in the pharmacokinetics of a new microemulsion formulation of cyclosporine in cardiac transplant recipients. Pharmacotherapy 18:364–70.
  • Chen M, Guan B, Xu H, et al. (2019). The molecular mechanism regulating diurnal rhythm of Flavin-containing monooxygenase 5 in mouse liver. Drug Metab Dispos. doi: 10.1124/dmd.119.088450.
  • Chu XY, Strauss JR, Mariano MA, et al. (2006). Characterization of mice lacking the multidrug resistance protein MRP2 (ABCC2). J Pharmacol Exp Ther 317:579–89.
  • Clench J, Reinberg A, Dziewanowska Z, et al. (1981). Circadian changes in the bioavailability and effects of indomethacin in healthy subjects. Eur J Clin Pharmacol 20:359–69.
  • Curtis AM, Bellet MM, Sassone-Corsi P, et al. (2014). Circadian clock proteins and immunity. Immunity 40:178–86.
  • Dallmann R, Brown SA, Gachon F. (2014). Chronopharmacology: new insights and therapeutic implications. Ann Rev Pharmacol Toxicol 54:339–61.
  • Damiola F, Le Minh N, Preitner N, et al. (2000). Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 14:2950–61.
  • DeBruyne JP, Weaver DR, Dallmann R. (2014). The hepatic circadian clock modulates xenobiotic metabolism in mice. J Biol Rhythms 29:277–87.
  • Deng J, Guo L, Wu B. (2018). Circadian regulation of hepatic cytochrome P450 2a5 by peroxisome proliferator-activated receptor γ. Drug Metab Dispos 46:1538–45.
  • Di Leo A, Gomez HL, Aziz Z, et al. (2008). Phase III, double-blind, randomized study comparing lapatinib plus paclitaxel with placebo plus paclitaxel as first-line treatment for metastatic breast cancer. J Clin Oncol 26:5544.
  • Dickens P, Tai YT, But PPH, et al. (1994). Fatal accidental aconitine poisoning following ingestion of Chinese herbal medicine: a report of two cases. Forensic Sci Int 67:55–8.
  • Dulong S, Ballesta A, Okyar A, et al. (2015). Identification of circadian determinants of cancer chronotherapy through in vitro chronopharmacology and mathematical modeling. Mol Cancer Ther 14:2154–64.
  • Endicott JA, Ling V. (1989). The biochemistry of P-glycoprotein-mediated multidrug resistance. Ann Rev Biochem 58:137–71.
  • Erol K, Kiliç FS, Batu ÖS, et al. (2001). Morning-evening administration time differences in digoxin kinetics in healthy young subjects. Chronobiol Int 18:841–9.
  • Feng D, Lazar MA. (2012). Clocks, metabolism, and the epigenome. Mol Cell 47:158–67.
  • Franken P, Dijk DJ. (2009). Circadian clock genes and sleep homeostasis. Eur J Neurosci 29:1820–9.
  • Gachon F, Olela FF, Schaad O, et al. (2006). The circadian PAR-domain basic leucine zipper transcription factors DBP, TEF, and HLF modulate basal and inducible xenobiotic detoxification. Cell Metab 4:25–36.
  • Gachon F, Firsov D. (2011). The role of circadian timing system on drug metabolism and detoxification. Exp Opin Drug Metab Toxicol 7:147–58.
  • Gorbacheva VY, Kondratov RV, Zhang R, et al. (2005). Circadian sensitivity to the chemotherapeutic agent cyclophosphamide depends on the functional status of the CLOCK/BMAL1 transactivation complex. Proc Natl Acad Sci 102:3407–12.
  • Guo L, Yu F, Zhang T, et al. (2018). The clock protein bmal1 regulates circadian expression and activity of sulfotransferase 1a1 in mice. Drug Metab Dispos 46:1403–10.
  • Hakkola J, Pasanen M, Purkunen R, et al. (1994). Expression of xenobiotic-metabolizing cytochrome P450 forms in human adult and fetal liver. Biochem Pharmacol 48:59–64.
  • Haus E, Fernandes G, Kuhl JF, et al. (1974). Murine circadian susceptibility rhythm to cyclophosphamide. Chronobiologia 1:270–7.
  • Heimbach T, Lakshminarayana SB, Hu W, et al. (2009). Practical anticipation of human efficacious doses and pharmacokinetics using in vitro and preclinical in vivo data. AAPS J 11:602.
  • Hishikawa S, Sugimoto K, Kobayashi E, et al. (2003). Dosing-time-dependent variation in biliary excretion of flomoxef in rats. Chronobiol Int 20:463–71.
  • Hughes S, Jagannath A, Hankins MW, et al. (2015). Photic regulation of clock systems. Methods Enzymol 552:125–43.
  • Innominato PF, Lévi FA, Bjarnason GA. (2010). Chronotherapy and the molecular clock: clinical implications in oncology. Adv Drug Deliv Rev 62:979–1001.
  • Ito K, Suzuki H, Horie T, et al. (2005). Apical/basolateral surface expression of drug transporters and its role in vectorial drug transport. Pharm Res 22:1559–77.
  • Iurisci I, Filipski E, Sallam H, et al. (2009). Liver circadian clock, a pharmacologic target of cyclin-dependent kinase inhibitor seliciclib. Chronobiol Int 26:1169–88.
  • Izukawa T, Nakajima M, Fujiwara R, et al. (2009). Quantitative analysis of UDP-glucuronosyltransferase (UGT) 1A and UGT2B expression levels in human livers. Drug Metab Dispos 37:1759–68.
  • Jancova P, Anzenbacher P, Anzenbacherova E. (2010). Phase II drug metabolizing enzymes. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 154:103–16.
  • Jedlitschky G, Hoffmann U, Kroemer HK. (2006). Structure and function of the MRP2 (ABCC2) protein and its role in drug disposition. Exp Opin Drug Metab Toxicol 2:351–66.
  • Kervezee L, Hartman R, van den Berg DJ, et al. (2017). Diurnal variation in the pharmacokinetics and brain distribution of morphine and its major metabolite. Eur J Pharm Sci 109:S132–S9.
  • Koyanagi S, Kuramoto Y, Nakagawa H, et al. (2003). A molecular mechanism regulating circadian expression of vascular endothelial growth factor in tumor cells. Cancer Res 63:7277–83.
  • Lamia KA, Storch KF, Weitz CJ. (2008). Physiological significance of a peripheral tissue circadian clock. Proc Natl Acad Sci 105:15172–7.
  • Lavery DJ, Lopez-Molina L, Margueron R, et al. (1999). Circadian expression of the steroid 15 α-hydroxylase (Cyp2a4) and coumarin 7-hydroxylase (Cyp2a5) genes in mouse liver is regulated by the PAR leucine zipper transcription factor DBP. Mol Cell Biol 19:6488–99.
  • Lévi F, Benavides M, Chevelle C, et al. (1990). Chemotherapy of advanced ovarian cancer with 4'-O-tetrahydropyranyl doxorubicin and cisplatin: a randomized phase II trial with an evaluation of circadian timing and dose-intensity. J Clin Oncol 8:705–14.
  • Lévi F. 2003. Circadian rhythms in 5-fluorouracil pharmacology and therapeutic applications. Fluoropyrimidines in cancer therapy. Totowa, NJ: Humana Press, 107–28.
  • Lévi F, Okyar A. (2011). Circadian clocks and drug delivery systems: impact and opportunities in chronotherapeutics. Exp Opin Drug Deliv 12:1535–41.
  • Lévi F, Schibler U. (2007). Circadian rhythms: mechanisms and therapeutic implications. Annu Rev Pharmacol Toxicol 47:593–628.
  • Lin Y, Zhou Z, Yang Z, et al. (2019). Circadian Cyp3a11 metabolism contributes to chronotoxicity of hypaconitine in mice. Chem Biol Interact 308:288.
  • Liu AC, Tran HG, Zhang EE, et al. (2008). Redundant function of REV-ERBalpha and beta and non-essential role for Bmal1 cycling in transcriptional regulation of intracellular circadian rhythms. PLoS Genet 4:e1000023.
  • Ma K, Xiao R, Tseng HT, et al. (2009). Circadian dysregulation disrupts bile acid homeostasis. PLoS One 4:e6843.
  • Malofeeva EV, Domanitskaya N, Gudima M, et al. (2012). Modulation of the ATPase and transport activities of broad-acting multidrug resistance factor ABCC10 (MRP7). Cancer Res 72:6457–67.
  • Masuda M, I’izuka Y, Yamazaki M, et al. (1997). Methotrexate is excreted into the bile by canalicular multispecific organic anion transporter in rats. Cancer Res 57:3506–10.
  • Matsunaga N, Ikeda M, Takiguchi T, et al. (2008). The molecular mechanism regulating 24-hour rhythm of CYP2E1 expression in the mouse liver. Hepatology 48:240–51.
  • Matsunaga N, Nakamura N, Yoneda N, et al. (2004). Influence of feeding schedule on 24-h rhythm of hepatotoxicity induced by acetaminophen in mice. J Pharmacol Exp Ther 311:594–600.
  • Mikkelsen TS, Thorn CF, Yang JJ, et al. (2011). PharmGKB summary: methotrexate pathway. Pharmacogenet Genom 21:679.
  • Mitsui S, Yamaguchi S, Matsuo T, et al. (2001). Antagonistic role of E4BP4 and PAR proteins in the circadian oscillatory mechanism. Genes Dev 15:995–1006.
  • Moore RY, Eichler VB. (1972). Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 42:201.
  • Motzer RJ, Hutson TE, Tomczak P, et al. (2007). Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med 356:115–24.
  • Mrosovsky N. (1996). Locomotor activity and non-photic influences on circadian clocks. Biol Rev 71:343–72.
  • Murakami Y, Higashi Y, Matsunaga N, et al. (2008). Circadian clock-controlled intestinal expression of the multidrug-resistance gene mdr1a in mice. Gastroenterology 135:1636–44.
  • Nair V, Casper R. (1969). The influence of light on daily rhythm in hepatic drug metabolizing enzymes in rat. Life Sci 8:1291–8.
  • Oda M, Koyanagi S, Tsurudome Y, et al. (2014). Renal circadian clock regulates the dosing-time dependency of cisplatin-induced nephrotoxicity in mice. Mol Pharmacol 85:715–22.
  • Oh JH, Lee JH, Han DH, et al. (2017). Circadian clock is involved in regulation of hepatobiliary transport mediated by multidrug resistance-associated protein 2. J Pharm Sci 106:2491–8.
  • Ohdo S, Inoue K, Yukawa E, et al. (1997a). Chronotoxicity of methotrexate in mice and its relation to circadian rhythm of DNA synthesis and pharmacokinetics. Jpn J Pharmacol 75:283–90.
  • Ohdo S, Makinosumi T, Ishizaki T, et al. (1997b). Cell cycle-dependent chronotoxicity of irinotecan hydrochloride in mice. J Pharmacol Exp Ther 283:1383–8.
  • Okamura A, Koyanagi S, Dilxiat A, et al. (2014). Bile acid-regulated peroxisome proliferator-activated receptor-α (PPARα) activity underlies circadian expression of intestinal peptide absorption transporter PepT1/Slc15a1. J Biol Chem 289:25296–305.
  • Okyar A, Kumar SA, Filipski E, et al. (2019). Sex-, feeding-, and circadian time-dependency of P-glycoprotein expression and activity-implications for mechanistic pharmacokinetics modeling. Sci Rep 9:10505.
  • Okyar A, Piccolo E, Ahowesso C, et al. (2011). Strain-and sex-dependent circadian changes in abcc2 transporter expression: implications for irinotecan chronotolerance in mouse ileum. PLoS One 6:e20393.
  • Paschos GK, Baggs JE, Hogenesch JB, et al. (2010). The role of clock genes in pharmacology. Ann Rev Pharmacol Toxicol 50:187–214.
  • Preitner N, Damiola F, Zakany J, et al. (2002). The orphan nuclear receptor Rev-erbalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110:251–60.
  • Prisant LM, Weber M, Black HR. (2003). The role of circadian rhythm in cardiovascular function-efficacy of a chronotherapeutic approach to controlling hypertension with Verelan® PM (verapamil HCl). Todays Ther Trends 21:201–14.
  • Radzialowski FM, Bousquet WF. (1968). Daily rhythmic variation in hepatic drug metabolism in the rat and mouse. J Pharmacol Exp Ther 163:229–38.
  • Rohman MS, Emoto N, Nonaka H, et al. (2005). Circadian clock genes directly regulate expression of the Na+/H+ exchanger NHE3 in the kidney. Kidney Int 67:1410–9.
  • Sahar S, Sassone-Corsi P. (2009). Metabolism and cancer: the circadian clock connection. Nat Rev Cancer 9:886.
  • Saito H, Terada T, Shimakura J, et al. (2008). Regulatory mechanism governing the diurnal rhythm of intestinal H+/peptide cotransporter 1 (PEPT1). Am J Physiol Gastrointest Liver Physiol 295:G395–G402.
  • Schinkel AH, Smit JJM, van Tellingen O, et al. (1994). Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 77:491–502.
  • Shepherd FA, Rodrigues Pereira J, Ciuleanu T, et al. (2005). Erlotinib in previously treated non–small-cell lung cancer. N Engl J Med 353:123–32.
  • Stearns AT, Balakrishnan A, Rhoads DB, et al. (2008). Diurnal rhythmicity in the transcription of jejunal drug transporters. J Pharmacol Sci 108:144.
  • Stupp R, Mason WP, Van Den Bent MJ, et al. (2005). Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–96.
  • Sukumaran S, Almon RR, DuBois DC, et al. (2010). Circadian rhythms in gene expression: relationship to physiology, disease, drug disposition and drug action. Adv Drug Deliv Rev 62:904–17.
  • Takeda N, Maemura K. (2011). Circadian clock and cardiovascular disease. J Cardiol 57:249–56.
  • Takiguchi T, Tomita M, Matsunaga N, et al. (2007). Molecular basis for rhythmic expression of CYP3A4 in serum-shocked HepG2 cells. Pharm Genom 17:1047–56.
  • Tanimura N, Kusunose N, Matsunaga N, et al. (2011). Aryl hydrocarbon receptor-mediated Cyp1a1 expression is modulated in a CLOCK-dependent circadian manner. Toxicology 290:203–7.
  • Testa B, Pedretti A, Vistoli G. (2012). Reactions and enzymes in the metabolism of drugs and other xenobiotics. Drug Discov Today 17:549–60.
  • Thaiss CA, Zeevi D, Levy M, et al. (2015). A day in the life of the meta-organism: diurnal rhythms of the intestinal microbiome and its host. Gut Microb 6:137–42.
  • Tibbitts J, Canter D, Graff R, et al. (2016). Key factors influencing ADME properties of therapeutic proteins: a need for ADME characterization in drug discovery and development. MAbs 8:229–45.
  • Tong Y, Zeng P, Zhang T, et al. (2019). The transcription factor E4bp4 regulates the expression and activity of Cyp3a11 in mice. Biochem Pharmacol 163:215–24.
  • Turek FW, Joshu C, Kohsaka A, et al. (2005). Obesity and metabolic syndrome in circadian Clock mutant mice. Science 308:1043–5.
  • Vagnerová K, Ergang P, Soták M, el al. (2019). Diurnal expression of ABC and SLC transporters in jejunum is modulated by adrenalectomy. Comp Biochem Physiol C Toxicol Pharmacol 226:108607.
  • Van De Waterbeemd H, Smith DA, Beaumont K, et al. (2001). Property-based design: optimization of drug absorption and pharmacokinetics. J Med Chem 44:1313–33.
  • Wada E, Koyanagi S, Kusunose N, et al. (2015). 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 87:314–22.
  • Wang S, Lin Y, Zhou Z, et al. (2019). Circadian clock gene bmal1 regulates bilirubin detoxification: a potential mechanism of feedback control of hyperbilirubinemia. Theranostics 9:5122–33.
  • Wang JF, Chou KC. (2010). Molecular modeling of cytochrome P450 and drug metabolism. Curr Drug Metab 11:342–6.
  • White CA, Pardue R, Huang C, et al. (1995). Chronobiological evaluation of the active biliary and renal secretion of ampicillin. Chronobiol Int 12:410–8.
  • Wood PA, Du-Quiton J, You S, et al. (2006). Circadian clock coordinates cancer cell cycle progression, thymidylate synthase, and 5-fluorouracil therapeutic index. Mol Cancer Ther 5:2023–33.
  • Xu C, Li CYT, Kong ANT. (2005). Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch Pharm Res 28:249.
  • Ye L, Wang T, Yang C, et al. (2011). Microsomal cytochrome P450-mediated metabolism of hypaconitine, an active and highly toxic constituent derived from Aconitum species. Toxicol Lett 204:81–91.
  • Yoo SH, Yamazaki S, Lowrey PL, et al. (2004). PERIOD2: LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci 101:5339–46.
  • Yu F, Zhang T, Zhou C, et al. (2019). The circadian clock gene bmal1 controls intestinal exporter MRP2 and drug disposition. Theranostics 9:2754.
  • Zhang T, Guo L, Yu F, et al. (2019). The nuclear receptor Rev-erbα participates in circadian regulation of Ugt2b enzymes in mice. Biochem Pharmacol 161:89–97.
  • Zhang T, Yu F, Guo L, et al. (2018). Small heterodimer partner regulates circadian cytochromes p450 and drug-induced hepatotoxicity. Theranostics 8:5246.
  • Zhao M, Zhang T, Yu F, et al. (2018). E4bp4 regulates carboxylesterase 2 enzymes through repression of the nuclear receptor Rev-erbα in mice. Biochem Pharmacol 152:293–301.
  • Zhao M, Zhao H, Deng J, et al. (2019). Role of the CLOCK protein in liver detoxification. Br J Pharmacol. doi: bph.14828/bph.14828.
  • Zhou Z, Lin Y, Gao L, et al. (2019a). Cyp3a11 metabolism-based chronotoxicity of brucine in mice. Toxicol Lett 313:188.
  • Zhou C, Yu F, Zeng P, et al. (2019b). Circadian sensitivity to the cardiac glycoside oleandrin is associated with diurnal intestinal P-glycoprotein expression. Biochem Pharmacol 169:113622.
  • Zmrzljak UP, Rozman D. (2012). Circadian regulation of the hepatic endobiotic and xenobitoic detoxification pathways: the time matters. Chem Res Toxicol 25:811–24.

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