Understanding circadian dynamics: current progress and future directions for chronobiology in drug discovery

References

• Zhang R, Lahens NF, Ballance HI, et al. A circadian gene expression atlas in mammals: implications for biology and medicine. Proc Natl Acad Sci U S A. 2014 Nov 11;111(45):16219–16224.
   PubMed Web of Science ®Google Scholar
• Mure LS, Le HD, Benegiamo G, et al. Diurnal transcriptome atlas of a primate across major neural and peripheral tissues. Science. 2018 Mar 16;359(6381). doi: 10.1126/science.aao0318
   PubMed Web of Science ®Google Scholar
• Ruben MD, Wu G, Smith DF, et al. A database of tissue-specific rhythmically expressed human genes has potential applications in circadian medicine. Sci Transl Med. 2018 Sep 12:10(458). doi: 10.1126/scitranslmed.aat8806
   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(6631):478–483. doi: 10.1126/science.add0846
   PubMed Web of Science ®Google Scholar
• Kramer A, Lange T, Spies C, et al. Foundations of circadian medicine. PLoS Biol. 2022;20(3):e3001567. doi: 10.1371/journal.pbio.3001567
   PubMed Web of Science ®Google Scholar
• Cederroth CR, Albrecht U, Bass J, et al. Medicine in the fourth dimension. Cell Metab. 2019;30(2):238–250. doi: 10.1016/j.cmet.2019.06.019
   PubMed Web of Science ®Google Scholar
• Klerman EB, Brager A, Carskadon MA, et al. Keeping an eye on circadian time in clinical research and medicine [10.1002/ctm2.1131]. Clinical & Translational Med. 2022 Dec 01;12(12):e1131.
   PubMed Web of Science ®Google Scholar
• Paul SM, Mytelka DS, Dunwiddie CT, et al. How to improve R&D productivity: the pharmaceutical industry’s grand challenge. Nat Rev Drug Discov. 2010 Mar;9(3):203–214.
   PubMed Web of Science ®Google Scholar
• Van Norman GA. Phase II trials in drug development and adaptive trial design. JACC Basic Transl Sci. 2019 Jun;4(3):428–437. doi: 10.1016/j.jacbts.2019.02.005
   PubMedGoogle Scholar
• Thomas DW, Burns J, Audette J, et al. Clinical development success rates 2006–2015. BIO Industry Analysis. 2016;1(16):25.
   Google Scholar
• Kaur G, Phillips C, Wong K, et al. Timing is important in medication administration: a timely review of chronotherapy research. Int J Clin Pharm. 2013 Jun;35(3):344–358.
   PubMed Web of Science ®Google Scholar
• Dallmann R, Brown SA, Gachon F. Chronopharmacology: new insights and therapeutic implications. Annu Rev Pharmacol Toxicol. 2014;54(1):339–361. doi:10.1146/annurev-pharmtox-011613-135923
   PubMedGoogle Scholar
• Leenaars CHC, Kouwenaar C, Stafleu FR, et al. Animal to human translation: a systematic scoping review of reported concordance rates. J Transl Med. 2019 Jul 15;17(1):223.
   PubMedGoogle Scholar
• Printezi MI, Kilgallen AB, Bond MJG, et al. Toxicity and efficacy of chronomodulated chemotherapy: a systematic review. Lancet Oncol. 2022;23(3):e129–e143. doi: 10.1016/S1470-2045(21)00639-2
   PubMed Web of Science ®Google Scholar
• Hermida RC, Ayala DE, Smolensky MH, et al. Chronotherapy with conventional blood pressure medications improves management of hypertension and reduces cardiovascular and stroke risks. Hypertens Res. 2016 May;39(5):277–292.
   PubMed Web of Science ®Google Scholar
• Scherholz ML, Schlesinger N, Androulakis IP. Chronopharmacology of glucocorticoids. Adv Drug Deliv Rev. 2019 Nov;151-152:245–261. doi: 10.1016/j.addr.2019.02.004
   PubMed Web of Science ®Google Scholar
• Gorbacheva VY, Kondratov RV, Zhang R, et al. Circadian sensitivity to the chemotherapeutic agent cyclophosphamide depends on the functional status of the CLOCK/BMAL1 transactivation complex. Proc Natl Acad Sci U S A. 2005 Mar 1;102(9):3407–3412. doi: 10.1073/pnas.0409897102
   PubMed Web of Science ®Google Scholar
• Manella G, Sabath E, Aviram R, et al. The liver-clock coordinates rhythmicity of peripheral tissues in response to feeding. Nat Metab. 2021 Jun;3(6):829–842.
   PubMedGoogle Scholar
• Greco CM, Koronowski KB, Smith JG, et al. Integration of feeding behavior by the liver circadian clock reveals network dependency of metabolic rhythms. Sci Adv. 2021 Sep 24;7(39):eabi7828.
   PubMed Web of Science ®Google Scholar
• Delbes AS, Quinones M, Gobet C, et al. Mice with humanized livers reveal the role of hepatocyte clocks in rhythmic behavior. Sci Adv. 2023 May 19;9(20):eadf2982.
   PubMed Web of Science ®Google Scholar
• Roenneberg T, Kantermann T, Juda M, et al. Light and the human circadian clock. Handb Exp Pharmacol. 2013;217:311–331.
   PubMedGoogle Scholar
• Stokkan KA, Yamazaki S, Tei H, et al. Entrainment of the circadian clock in the liver by feeding. Science. 2001 Jan 19;291(5503):490–493. doi: 10.1126/science.291.5503.490
   PubMed Web of Science ®Google Scholar
• Damiola F, Le Minh N, Preitner N, et al. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 2000 Dec 1;14(23):2950–2961. doi: 10.1101/gad.183500
   PubMed Web of Science ®Google Scholar
• Atger F, Mauvoisin D, Weger B, et al. Regulation of mammalian physiology by interconnected circadian and feeding rhythms [Review]. Front Endocrinol. 2017;8:42. doi: 10.3389/fendo.2017.00042
   PubMed Web of Science ®Google Scholar
• Challet E. The circadian regulation of food intake. Nat Rev Endocrinol. 2019 Jul;15(7):393–405. doi: 10.1038/s41574-019-0210-x
   PubMed Web of Science ®Google Scholar
• Nagai K, Nishio T, Nakagawa H, et al. Effect of bilateral lesions of the suprachiasmatic nuclei on the circadian rhythm of food-intake. Brain Res. 1978 Feb 24;142(2):384–389.
   PubMed Web of Science ®Google Scholar
• Lamia KA, Storch KF, Weitz CJ. Physiological significance of a peripheral tissue circadian clock. Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15172–15177.
   PubMed Web of Science ®Google Scholar
• Vollmers C, Gill S, DiTacchio L, et al. Time of feeding and the intrinsic circadian clock drive rhythms in hepatic gene expression. Proc Natl Acad Sci U S A. 2009 Dec 15;106(50):21453–21458. doi: 10.1073/pnas.0909591106
   PubMed Web of Science ®Google Scholar
• Adamovich Y, Rousso-Noori L, Zwighaft Z, et al. Circadian clocks and feeding time regulate the oscillations and levels of hepatic triglycerides. Cell Metab. 2014 Feb 4;19(2):319–330.
   PubMed Web of Science ®Google Scholar
• Turek FW, Joshu C, Kohsaka A, et al. Obesity and metabolic syndrome in circadian clock mutant mice. Science. 2005 May 13;308(5724):1043–1045.
   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 Jan 19;118(3). doi: 10.1073/pnas.2015803118
   PubMed Web of Science ®Google Scholar
• Patke A, Young MW, Axelrod S. Molecular mechanisms and physiological importance of circadian rhythms. Nat Rev Mol Cell Biol. 2020 Feb 01;21(2):67–84.
   PubMed Web of Science ®Google Scholar
• Rijo-Ferreira F, Takahashi JS. Genomics of circadian rhythms in health and disease. Genome Med. 2019 Dec 17;11(1):82.
   PubMed Web of Science ®Google Scholar
• Takahashi JS. Transcriptional architecture of the mammalian circadian clock. Nat Rev Genet. 2017 Mar;18(3):164–179. doi: 10.1038/nrg.2016.150
   PubMed Web of Science ®Google Scholar
• Gachon F, Leuenberger N, Claudel T, et al. Proline- and acidic amino acid-rich basic leucine zipper proteins modulate peroxisome proliferator-activated receptor α (PPARα) activity. Proc Natl Acad Sci U S A. 2011 Mar 22;108(12):4794–4799.
   PubMed Web of Science ®Google Scholar
• Cretenet G, Le Clech M, Gachon F. Circadian clock-coordinated 12 hr period rhythmic activation of the ire1a pathway controls lipid metabolism in mouse liver. Cell Metab. 2010;11(1):47–57. doi: 10.1016/j.cmet.2009.11.002
   PubMed Web of Science ®Google Scholar
• Jouffe C, Cretenet G, Symul L, et al. The circadian clock coordinates ribosome biogenesis. PLoS Biol. 2013;11(1):e1001455. doi: 10.1371/journal.pbio.1001455
   PubMed Web of Science ®Google Scholar
• Sinturel F, Gerber A, Mauvoisin D, et al. Diurnal oscillations in liver mass and cell size accompany ribosome assembly cycles. Cell. 2017;169(4):651–663.e14. doi: 10.1016/j.cell.2017.04.015
   PubMed Web of Science ®Google Scholar
• Atger F, Gobet C, Marquis J, et al. Circadian and feeding rhythms differentially affect rhythmic mRNA transcription and translation in mouse liver. Proc Natl Acad Sci U S A. 2015 Nov 24;112(47):E6579–88.
   PubMed Web of Science ®Google Scholar
• Wang J, Mauvoisin D, Martin E, et al. Nuclear proteomics uncovers diurnal regulatory landscapes in mouse liver. Cell Metab. 2017 Jan 10;25(1):102–117.
   PubMed Web of Science ®Google Scholar
• Mauvoisin D, Wang J, Jouffe C, et al. Circadian clock-dependent and -independent rhythmic proteomes implement distinct diurnal functions in mouse liver. Proc Natl Acad Sci U S A. 2014 Jan 7;111(1):167–172.
   PubMed Web of Science ®Google Scholar
• Weger M, Weger BD, Gachon F. The mechanisms and physiological consequences of diurnal hepatic cell size fluctuations: a brief review. Cell Physiol Biochem. 2022 Jan 15;56(S2):1–11.
   PubMedGoogle Scholar
• Bignon Y, Wigger L, Ansermet C, et al. Multiomics reveals multilevel control of renal and systemic metabolism by the renal tubular circadian clock. J Clin Invest. 2023 Mar 02;133. doi: 10.1172/JCI167133
   PubMed Web of Science ®Google Scholar
• Panda S, Antoch MP, Miller BH, et al. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell. 2002 May 3;109(3):307–320.
   PubMed Web of Science ®Google Scholar
• Zuber AM, Centeno G, Pradervand S, et al. Molecular clock is involved in predictive circadian adjustment of renal function. Proc Natl Acad Sci U S A. 2009 Sep 22;106(38):16523–16528.
   PubMed Web of Science ®Google Scholar
• Johnson BP, Walisser JA, Liu Y, et al. Hepatocyte circadian clock controls acetaminophen bioactivation through NADPH-cytochrome P450 oxidoreductase. Proc Natl Acad Sci U S A. 2014;111(52):18757–18762. doi: 10.1073/pnas.1421708111
   PubMed Web of Science ®Google Scholar
• Kang HS, Angers M, Beak JY, et al. Gene expression profiling reveals a regulatory role for ROR alpha and ROR gamma in phase I and phase II metabolism. Physiol Genomics. 2007 Oct 22;31(2):281–294.
   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 Apr 15;15(8):995–1006.
   PubMed Web of Science ®Google Scholar
• Gachon F, Fleury Olela F, 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 Jul;4(1):25–36. doi: 10.1016/j.cmet.2006.04.015
   PubMed Web of Science ®Google Scholar
• Murakami Y, Higashi Y, Matsunaga N, et al. Circadian clock-controlled intestinal expression of the multidrug-resistance gene mdr1a in mice. Gastroenterology. 2008 Nov;135(5):1636–1644 e3.
   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
• DeBruyne JP, Weaver DR, Dallmann R. The hepatic circadian clock modulates xenobiotic metabolism in mice. J Biol Rhythms. 2014 Aug;29(4):277–287. doi: 10.1177/0748730414544740
   PubMed Web of Science ®Google Scholar
• Ransick A, Lindström NO, Liu J, et al. Single-cell profiling reveals sex, lineage, and regional diversity in the mouse kidney. Dev Cell. 2019 Nov 04;51(3):399–413.e7.
   PubMed Web of Science ®Google Scholar
• Yang X, Schadt EE, Wang S, et al. Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res. 2006;16(8):995–1004. doi: 10.1101/gr.5217506
   PubMed Web of Science ®Google Scholar
• Brie B, Ramirez MC, De Winne C, et al. Brain control of sexually dimorphic liver function and disease: the endocrine connection. Cell Mol Neurobiol. 2019 Mar 01;39(2):169–180.
   PubMed Web of Science ®Google Scholar
• Toews JNC, Hammond GL, Viau V. Liver at the nexus of rat postnatal HPA axis maturation and sexual dimorphism. J Endocrinol. 2021 Jan 01;248(1):R1–R17.
   PubMed Web of Science ®Google Scholar
• Laouari D, Vergnaud P, Hirose T, et al. The sexual dimorphism of kidney growth in mice and humans. Kidney Int. 2022 Jul 01;102(1):78–95.
   PubMed Web of Science ®Google Scholar
• Miller MA. Gender-based differences in the toxicity of pharmaceuticals—the food and drug administration’s perspective. Int J Toxicol. 2001 May 01;20(3):149–152.
   PubMed Web of Science ®Google Scholar
• Nicolson TJ, Mellor HR, Roberts RRA. Gender differences in drug toxicity. Trends Pharmacol Sci. 2010 Mar 01;31(3):108–114.
   PubMed Web of Science ®Google Scholar
• Özdemir BC, Gerard CL, Espinosa da Silva C. Sex and gender differences in anticancer treatment toxicity: a call for revisiting drug dosing in oncology. Endocrinology. 2022;163(6):bqac058. doi: 10.1210/endocr/bqac058
   PubMed Web of Science ®Google Scholar
• Noghrehchi F, Dawson AH, Raubenheimer JE, et al. Role of age-sex as underlying risk factors for death in acute pesticide self-poisoning: a prospective cohort study. Clin Toxicol (Phila). 2022 Feb 01;60(2):184–190.
   PubMed Web of Science ®Google Scholar
• Beauchamp GA, Carey JL, Adams T, et al. Sex differences in poisonings among older adults: an analysis of the toxicology investigators consortium (ToxIC) registry, 2010 to 2016. Clin Ther. 2018 Aug 01;40(8):1366–1374.e8.
   PubMed Web of Science ®Google Scholar
• Petrushevska T, Jakovski Z, Poposka V, et al. Drug-related deaths between 2002 and 2013 with accent to methadone and benzodiazepines. J Forensic Leg Med. 2015 Apr 01;31:12–18.
   PubMed Web of Science ®Google Scholar
• Layton AT, Gumz ML. Sex differences in circadian regulation of kidney function of the mouse. Am J Physiol Renal Physiol. 2022 Dec 01;323(6):F675–F685.
   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 Feb 5;29(2):362–382.e8. doi: 10.1016/j.cmet.2018.09.023
   PubMed Web of Science ®Google Scholar
• Ahowesso C, Li X-M, Zampera S, et al. Sex and dosing-time dependencies in irinotecan-induced circadian disruption. Chronobiol Int. 2011 May 01;28(5):458–470.
   PubMed Web of Science ®Google Scholar
• Bon K, Lantéri-Minet M, Menétrey D, et al. Sex, time-of-day and estrous variations in behavioral and bladder histological consequences of cyclophosphamide-induced cystitis in rats. Pain. 1997;73(3):423–429. doi: 10.1016/S0304-3959(97)00134-6
   PubMed Web of Science ®Google Scholar
• Lawrence GM, Beesley AC. The effect of diurnal rhythms on the hepatotoxicity of thioacetamide in male and female rats. Drug Metabol Drug Interact. 1988;6(3–4):359–370. doi: 10.1515/DMDI.1988.6.3-4.359
   PubMedGoogle Scholar
• Giacchetti S, Dugué PA, Innominato PF, et al. Sex moderates circadian chemotherapy effects on survival of patients with metastatic colorectal cancer: a meta-analysis. Ann Oncol. 2012;23(12):3110–3116. doi: 10.1093/annonc/mds148
   PubMed Web of Science ®Google Scholar
• Li X-M, Mohammad-Djafari A, Dumitru M, et al. A circadian clock transcription model for the personalization of cancer chronotherapy. Cancer Res. 2013;73(24):7176–7188. doi: 10.1158/0008-5472.CAN-13-1528
   PubMed Web of Science ®Google Scholar
• Innominato PF, Ballesta A, Huang Q, et al. Sex-dependent least toxic timing of irinotecan combined with chronomodulated chemotherapy for metastatic colorectal cancer: randomized multicenter EORTC 05011 trial [10.1002/cam4.3056]. Cancer Med. 2020 Jun 01;9(12):4148–4159. doi: 10.1002/cam4.3056
   PubMed Web of Science ®Google Scholar
• Kim DW, Byun JM, Lee J-O, et al. Chemotherapy delivery time affects treatment outcomes of female patients with diffuse large B-cell lymphoma. JCI Insight. 2022 Dec 13;8. doi: 10.1172/jci.insight.164767
   Web of Science ®Google Scholar
• Ghoneim RH, Ngo Sock ET, Lavoie J-M, et al. Effect of a high-fat diet on the hepatic expression of nuclear receptors and their target genes: relevance to drug disposition. Br J Nutr. 2015;113(3):507–516. doi: 10.1017/S0007114514003717
   PubMed Web of Science ®Google Scholar
• Ning M, Jeong H. High-fat diet feeding alters expression of hepatic drug-metabolizing enzymes in mice. Drug Metab Dispos. 2017;45(7):707–711. doi: 10.1124/dmd.117.075655
   PubMed Web of Science ®Google Scholar
• Brill MJE, Diepstraten J, van Rongen A, et al. Impact of obesity on drug metabolism and elimination in adults and children. Clin Pharmacokinet. 2012 May 01;51(5):277–304.
   PubMed Web of Science ®Google Scholar
• Mikhailova ON, Gulyaeva LF, Filipenko ML. Gene expression of drug metabolizing enzymes in adult and aged mouse liver: a modulation by immobilization stress. Toxicology. 2005;210(2–3):189–196. doi: 10.1016/j.tox.2005.01.018
   PubMed Web of Science ®Google Scholar
• Oshida K, Waxman DJ, Corton JC, et al. Chemical and hormonal effects on STAT5b-dependent sexual dimorphism of the liver transcriptome. PLoS ONE. 2016;11(3):e0150284. doi: 10.1371/journal.pone.0150284
   PubMed Web of Science ®Google Scholar
• Oshida K, Vasani N, Waxman DJ, et al. Disruption of STAT5b-regulated sexual dimorphism of the liver transcriptome by diverse factors is a common event. PLoS ONE. 2016;11(3):e0148308. doi: 10.1371/journal.pone.0148308
   PubMed Web of Science ®Google Scholar
• Rasmussen MH, Hvidberg A, Juul A, et al. Massive weight loss restores 24-hour growth hormone release profiles and serum insulin-like growth factor-I levels in obese subjects. J Clin Endocrinol Metab. 1995;80(4):1407–1415. doi: 10.1210/jcem.80.4.7536210
   PubMed Web of Science ®Google Scholar
• Huang L, Steyn FJ, Tan HY, et al. The decline in pulsatile GH Secretion throughout early adulthood in mice is exacerbated by dietary-induced weight gain. Endocrinology. 2012;153(9):4380–4388. doi: 10.1210/en.2012-1178
   PubMed Web of Science ®Google Scholar
• Giustina A, Veldhuis JD. Pathophysiology of the neuroregulation of growth hormone secretion in experimental animals and the human. Endocr Rev. 1998 Dec 1;19(6):717–797.
   PubMed Web of Science ®Google Scholar
• Jouffe C, Weger Benjamin D, Martin E, et al. Disruption of the circadian clock component BMAL1 elicits an endocrine adaption impacting on insulin sensitivity and liver disease. Proc Natl Acad Sci U S A. 2022 Mar 08;119(10):e2200083119.
   PubMed Web of Science ®Google Scholar
• Buckley TN, Omotola O, Archer LA, et al. High-fat feeding disrupts daily eating behavior rhythms in obesity-prone but not in obesity-resistant male inbred mouse strains. Am J Physiol Regul Integr Comp Physiol. 2021 May 01;320(5):R619–R629.
   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
• Hatori M, Vollmers C, Zarrinpar A, et al. Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab. 2012 Jun 6;15(6):848–860.
   PubMed Web of Science ®Google Scholar
• Nakamura TJ, Nakamura W, Yamazaki S, et al. Age-related decline in circadian output. J Neurosci. 2011;31(28):10201–10205. doi: 10.1523/JNEUROSCI.0451-11.2011
   PubMed Web of Science ®Google Scholar
• Acosta-Rodríguez V, Rijo-Ferreira F, Izumo M, et al. Circadian alignment of early onset caloric restriction promotes longevity in male C57BL/6J mice. Science. 2022 Jun 10;376(6598):1192–1202.
   PubMed Web of Science ®Google Scholar
• Hanley MJ, Abernethy DR, Greenblatt DJ. Effect of obesity on the pharmacokinetics of drugs in humans. Clin Pharmacokinet. 2010 Feb 01;49(2):71–87.
   PubMed Web of Science ®Google Scholar
• Mangoni AA, Jackson SH. Age-related changes in pharmacokinetics and pharmacodynamics: basic principles and practical applications. Br J Clin Pharmacol. 2004 Jan;57(1):6–14. doi: 10.1046/j.1365-2125.2003.02007.x
   PubMed Web of Science ®Google Scholar
• Vinarov Z, Abdallah M, Agundez JAG, et al. Impact of gastrointestinal tract variability on oral drug absorption and pharmacokinetics: an UNGAP review. Eur J Pharm Sci. 2021 Jul 1;162:105812.
   PubMed Web of Science ®Google Scholar
• Matsunaga N, Nakamura N, Yoneda N, et al. Influence of feeding schedule on 24-h rhythm of hepatotoxicity induced by acetaminophen in mice. J Pharmacol Exp Ther. 2004 Nov;311(2):594–600.
   PubMed Web of Science ®Google Scholar
• Song JG, Nakano S, Ohdo S, et al. Chronotoxicity and chronopharmacokinetics of methotrexate in mice: modification by feeding schedule. Jpn J Pharmacol. 1993 Aug;62(4):373–378.
   PubMedGoogle Scholar
• Song J, Ohdo S, Ogawa N, et al. Influence of feeding schedule on chronopharmacological aspects of gentamicin in mice. Chronobiol Int. 1993 Oct;10(5):338–348.
   PubMed Web of Science ®Google Scholar
• Ohdo S, Nakano S, Ogawa N. Chronopharmacological study of sodium valproate in mice: dose-concentration-response relationship. Jpn J Pharmacol. 1988 May;47(1):11–19. doi: 10.1016/S0021-5198(19)43245-9
   PubMedGoogle Scholar
• Toulis KA, Nirantharakumar K, Pourzitaki C, et al. Glucokinase activators for type 2 diabetes: challenges and future developments. Drugs. 2020 Apr;80(5):467–475.
   PubMed Web of Science ®Google Scholar
• Kim YC, Lee SJ. Temporal variation in hepatotoxicity and metabolism of acetaminophen in mice. Toxicology. 1998 Jun 26;128(1):53–61.
   PubMed Web of Science ®Google Scholar
• Marcheva B, Ramsey KM, Buhr ED, et al. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature. 2010 Jul 29;466(7306):627–631.
   PubMed Web of Science ®Google Scholar
• Kroon T, Hagstedt T, Alexandersson I, et al. Chronotherapy with a glucokinase activator profoundly improves metabolism in obese Zucker rats. Sci, trans med. 2022;14(668):eabh1316. doi: 10.1126/scitranslmed.abh1316
   PubMed Web of Science ®Google Scholar
• Weger BD, Rawashdeh O, Gachon F. At the intersection of microbiota and circadian clock: are sexual dimorphism and growth hormones the missing link to pathology?: circadian clock and microbiota: potential egffect on growth hormone and sexual development. BioEssays. 2019 Sep;41(9):e1900059. doi: 10.1002/bies.201900059
   PubMed Web of Science ®Google Scholar
• Litichevskiy L, Thaiss CA. The oscillating gut microbiome and its effects on host circadian biology. Annu Rev Nutr. 2022 Aug 22;42(1):145–164.
   PubMedGoogle Scholar
• Thaiss CA, Zeevi D, Levy M, et al. Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell. 2014 Oct 23;159(3):514–529. doi: 10.1016/j.cell.2014.09.048
   PubMed Web of Science ®Google Scholar
• Thaiss CA, Levy M, Korem T, et al. Microbiota diurnal rhythmicity programs host transcriptome oscillations. Cell. 2016 Dec 1;167(6):1495–1510 e12. doi: 10.1016/j.cell.2016.11.003
   PubMed Web of Science ®Google Scholar
• Skarke C, Lahens NF, Rhoades SD, et al. A pilot characterization of the human chronobiome. Sci Rep. 2017 Dec 7;7(1):17141.
   PubMedGoogle Scholar
• Ellison AR, Wilcockson D, Cable J. Circadian dynamics of the teleost skin immune-microbiome interface. Microbiome. 2021 Nov 16;9(1):222.
   PubMed Web of Science ®Google Scholar
• Brooks JF 2nd, Behrendt CL, Ruhn KA, et al. The microbiota coordinates diurnal rhythms in innate immunity with the circadian clock. Cell. 2021 Aug 5;184(16):4154–4167 e12.
   PubMed Web of Science ®Google Scholar
• Zarrinpar A, Chaix A, Yooseph S, et al. Diet and feeding pattern affect the diurnal dynamics of the gut microbiome. Cell Metab. 2014 Dec 2;20(6):1006–1017. doi: 10.1016/j.cmet.2014.11.008
   PubMed Web of Science ®Google Scholar
• Leeming ER, Louca P, Gibson R, et al. The complexities of the diet-microbiome relationship: advances and perspectives. Genome Med. 2021 Jan 20;13(1):10.
   PubMed Web of Science ®Google Scholar
• Hildebrand F, Nguyen TL, Brinkman B, et al. Inflammation-associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice. Genome Biol. 2013 Jan 24;14(1):R4.
   PubMed Web of Science ®Google Scholar
• Rothschild D, Weissbrod O, Barkan E, et al. Environment dominates over host genetics in shaping human gut microbiota. Nature. 2018 Mar 8;555(7695):210–215.
   PubMed Web of Science ®Google Scholar
• Heddes M, Altaha B, Niu Y, et al. The intestinal clock drives the microbiome to maintain gastrointestinal homeostasis. Nat Commun. 2022 Oct 14;13(1):6068.
   PubMed Web of Science ®Google Scholar
• Leone V, Gibbons SM, Martinez K, et al. Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism. Cell Host Microbe. 2015 May 13;17(5):681–689.
   PubMed Web of Science ®Google Scholar
• Jensen TL, Kiersgaard MK, Sorensen DB, et al. Fasting of mice: a review. Lab Anim. 2013 Oct;47(4):225–240.
   PubMed Web of Science ®Google Scholar
• Spanogiannopoulos P, Bess EN, Carmody RN, et al. The microbial pharmacists within us: a metagenomic view of xenobiotic metabolism. Nat Rev Microbiol. 2016 Apr;14(5):273–287.
   PubMed Web of Science ®Google Scholar
• Zimmermann M, Zimmermann-Kogadeeva M, Wegmann R, et al. Mapping human microbiome drug metabolism by gut bacteria and their genes. Nature. 2019 Jun 01;570(7762):462–467. doi: 10.1038/s41586-019-1291-3
   PubMed Web of Science ®Google Scholar
• Lee JH, Lee J. Indole as an intercellular signal in microbial communities. FEMS Microbiol Rev. 2010 Jul;34(4):426–444. doi: 10.1111/j.1574-6976.2009.00204.x
   PubMed Web of Science ®Google Scholar
• Tintelnot J, Xu Y, Lesker TR, et al. Microbiota-derived 3-IAA influences chemotherapy efficacy in pancreatic cancer. Nature. 2023 Mar 01;615(7950):168–174. doi: 10.1038/s41586-023-05728-y
   PubMed Web of Science ®Google Scholar
• Paulose JK, Wright JM, Patel AG, et al. Human gut bacteria are sensitive to melatonin and express endogenous circadian rhythmicity. PLoS ONE. 2016;11(1):e0146643. doi: 10.1371/journal.pone.0146643
   PubMed Web of Science ®Google Scholar
• Paulose JK, Cassone CV, Graniczkowska KB, et al. Entrainment of the circadian clock of the enteric bacterium Klebsiella aerogenes by temperature cycles. iScience. 2019 Sep 27;19:1202–1213.
   PubMed Web of Science ®Google Scholar
• Eelderink-Chen Z, Bosman J, Sartor F, et al. A circadian clock in a nonphotosynthetic prokaryote. Sci Adv. 2021 Jan;7(2). doi: 10.1126/sciadv.abe2086
   PubMed Web of Science ®Google Scholar
• Nelson RJ, Bumgarner JR, Liu JA, et al. Time of day as a critical variable in biology. BMC Biol. 2022 Jun 15;20(1):142.
   PubMed Web of Science ®Google Scholar
• Esposito E, Li WT, Mandeville E, et al. Potential circadian effects on translational failure for neuroprotection. Nature. 2020 Jun 01;582(7812):395–398.
   PubMed Web of Science ®Google Scholar