1,196
Views
55
CrossRef citations to date
0
Altmetric
Review

Circadian rhythms: a regulator of gastrointestinal health and dysfunction

, &
Pages 411-424 | Received 10 Sep 2018, Accepted 12 Mar 2019, Published online: 25 Mar 2019

References

  • Mohawk JA, Green CB, Takahashi JS. Central and peripheral circadian clocks in mammals. Aliment Ann Rev Neurosci. 2012;35:445–462.
  • Duffy JF, Cain SW, Chang AM, et al. Sex difference in the near-24-hour intrinsic period of the human circadian timing system. Proc Natl Acad Sci U S A. 2011;108(Suppl 3):15602–15608.
  • Konturek PC, Brzozowski T, Konturek SJ. Gut clock: implication of circadian rhythms in the gastrointestinal tract. J Physiol Pharmacol. 2011;62(2):139–150.
  • Hoogerwerf WA. Role of biological rhythms in gastrointestinal health and disease. Rev Endocr Metab Disord. 2009;10(4):293–300.
  • Roenneberg T, Allebrandt KV, Merrow M, et al. Social jetlag and obesity. Curr Biol. 2012;22(10):939–943.
  • Sulli G, Manoogian ENC, Taub PR, et al. Training the circadian clock, clocking the drugs, and drugging the clock to prevent, manage, and treat chronic diseases. Trends Pharmacol Sci. 2018;39(9):812–827.
  • Heitkemper M, Jarrett M, Burr R, et al. Subjective and objective sleep indices in women with irritable bowel syndrome. Neurogastroenterol Motil. 2005;17(4):523–530.
  • Rotem AY, Sperber AD, Krugliak P, et al. Polysomnographic and actigraphic evidence of sleep fragmentation in patients with irritable bowel syndrome. Sleep. 2003;26(6):747–752.
  • Elsenbruch S, Harnish MJ, Orr WC. Subjective and objective sleep quality in irritable bowel syndrome. Am J Gastroenterol. 1999;94(9):2447–2452.
  • Patel A, Hasak S, Cassell B, et al. Effects of disturbed sleep on gastrointestinal and somatic pain symptoms in irritable bowel syndrome. Pharmacol Ther. 2016;44(3):246–258.
  • Buchanan DT, Cain K, Heitkemper M, et al. Sleep measures predict next-day symptoms in women with irritable bowel syndrome. J Clin Sleep Med. 2014;10(9):1003–1009.
  • Nojkov B, Rubenstein JH, Chey WD, et al. The impact of rotating shift work on the prevalence of irritable bowel syndrome in nurses. Am J Gastroenterol. 2010;105(4):842–847.
  • Caruso CC, Lusk SL, Gillespie BW. Relationship of work schedules to gastrointestinal diagnoses, symptoms, and medication use in auto factory workers. Am J Ind Med. 2004;46(6):586–598.
  • Kim HI, Jung SA, Choi JY, et al. Impact of shiftwork on irritable bowel syndrome and functional dyspepsia. J Korean Med Sci. 2013;28(3):431–437.
  • Zhen LW, Ann GK, Yu HK. Functional bowel disorders in rotating shift nurses may be related to sleep disturbances. Eur J Gastroenterol Hepatol. 2006;18(6):623–627.
  • Basnet S, Merikanto I, Lahti T, et al. Associations of common noncommunicable medical conditions and chronic diseases with chronotype in a population-based health examination study. Chronobiol Int. 2017;34(4):462–470.
  • Saini C, Brown SA, Dibner C. Human peripheral clocks: applications for studying circadian phenotypes in physiology and pathophysiology. Front Neurol. 2015;6:95.
  • Swanson GR, Burgess HJ, Keshavarzian A. Sleep disturbances and inflammatory bowel disease: a potential trigger for disease flare? Expert Rev Clin Immunol. 2011;7(1):29–36.
  • Swanson GR, Burgess HJ. Sleep and circadian hygiene and inflammatory bowel disease. Gastroenterol Clin North Am. 2017;46(4):881–893.
  • Hoogerwerf WA. Biologic clocks and the gut. Curr Gastroenterol Rep. 2006;8(5):353–359.
  • Scheving LA. Biological clocks and the digestive system. Gastroenterology. 2000;119(2):536–549.
  • Hoogerwerf WA, Hellmich HL, Cornelissen G, et al. Clock gene expression in the murine gastrointestinal tract: endogenous rhythmicity and effects of a feeding regimen. Gastroenterology. 2007;133(4):1250–1260.
  • Stokes K, Cooke A, Chang H, et al. The circadian clock gene bmal1 coordinates intestinal regeneration. Cell Mol Gastroenterol Hepatol. 2017;4(1):95–114.
  • Yoshida D, Aoki N, Tanaka M, et al. The circadian clock controls fluctuations of colonic cell proliferation during the light/dark cycle via feeding behavior in mice. Chronobiol Int. 2015;32(8):1145–1155.
  • Wang Q, Ao Y, Yang K, et al. Circadian clock gene per2 plays an important role in cell proliferation, apoptosis and cell cycle progression in human oral squamous cell carcinoma. Oncol Rep. 2016;35(6):3387–3394.
  • Wang Y, Qian R, Sun N, et al. Circadian gene hclock enhances proliferation and inhibits apoptosis of human colorectal carcinoma cells in vitro and in vivo. Mol Med Rep. 2015;11(6):4204–4210.
  • Hoogerwerf WA. Role of clock genes in gastrointestinal motility. Am J Physiol Gastrointest Liver Physiol. 2010;299(3):G549–G55.
  • Hoogerwerf WA, Shahinian VB, Cornelissen G, et al. Rhythmic changes in colonic motility are regulated by period genes. Am J Physiol Gastrointest Liver Physiol. 2010;298(2):G143–G50.
  • Yamaguchi M, Kotani K, Tsuzaki K, et al. Circadian rhythm genes clock and per3 polymorphisms and morning gastric motility in humans. PLoS One. 2015;10(3):e0120009.
  • 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–G402.
  • Okamura A, Koyanagi S, Dilxiat A, et al. Bile acid-regulated peroxisome proliferator-activated receptor-alpha (pparalpha) activity underlies circadian expression of intestinal peptide absorption transporter pept1/slc15a1. J Biol Chem. 2014;289(36):25296–25305.
  • Sladek M, Rybova M, Jindrakova Z, et al. Insight into the circadian clock within rat colonic epithelial cells. Gastroenterology. 2007;133(4):1240–1249.
  • Qandeel HG, Duenes JA, Zheng Y, et al. Diurnal expression and function of peptide transporter 1 (pept1). J Surg Res. 2009;156(1):123–128.
  • Pan X, Terada T, Okuda M, et al. The diurnal rhythm of the intestinal transporters sglt1 and pept1 is regulated by the feeding conditions in rats. J Nutr. 2004;134(9):2211–2215.
  • Saifur RM, Emoto N, Nonaka H, et al. Circadian clock genes directly regulate expression of the na(+)/h(+) exchanger nhe3 in the kidney. Kidney Int. 2005;67(4):1410–1419.
  • Pacha J, Sumova A. Circadian regulation of epithelial functions in the intestine. Acta Physiol (Oxf). 2013;208(1):11–24.
  • 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.
  • Wong PM, Hasler BP, Kamarck TW, et al. Social jetlag, chronotype, and cardiometabolic risk. J Clin Endocrinol Metab. 2015;100(12):4612–4620.
  • Hussain MM, Pan X. Circadian regulators of intestinal lipid absorption. J Lipid Res. 2015;56(4):761–770.
  • Pan X, Munshi MK, Iqbal J, et al. Circadian regulation of intestinal lipid absorption by apolipoprotein aiv involves forkhead transcription factors a2 and o1 and microsomal triglyceride transfer protein. J Biol Chem. 2013;288(28):20464–20476.
  • Firsov D, Tokonami N, Bonny O. Role of the renal circadian timing system in maintaining water and electrolytes homeostasis. Mol Cell Endocrinol. 2012;349(1):51–55.
  • Hilfenhaus M. Circadian rhythm of the renin-angiotensin-aldosterone system in the rat. Arch Toxicol. 1976;36(3–4):305–316.
  • Voigt RM, Forsyth CB, Shaikh M, et al. Diurnal variations in intestinal barrier integrity and liver pathology in mice: implications for alcohol binge. Am J Physiol Gastrointest Liver Physiol. 2018;314(1):G131–G41.
  • Kyoko OO, Kono H, Ishimaru K, et al. Expressions of tight junction proteins occludin and claudin-1 are under the circadian control in the mouse large intestine: implications in intestinal permeability and susceptibility to colitis. PLoS One. 2014;9(5):e98016.
  • Summa KC, Voigt RM, Forsyth CB, et al. Disruption of the circadian clock in mice increases intestinal permeability and promotes alcohol-induced hepatic pathology and inflammation. PLoS One. 2013;8(6):e67102.
  • Swanson GR, Gorenz A, Shaikh M, et al. Night workers with circadian misalignment are susceptible to alcohol-induced intestinal hyperpermeability with social drinking. Am J Physiol Gastrointest Liver Physiol. 2016;311(1):G192–G201.
  • Swanson G, Forsyth CB, Tang Y, et al. Role of intestinal circadian genes in alcohol-induced gut leakiness. Alcohol Clin Exp Res. 2011;35(7):1305–1314.
  • Bishehsari F, Saadalla A, Khazaie K, et al. Light/dark shifting promotes alcohol-induced colon carcinogenesis: possible role of intestinal inflammatory milieu and microbiota. Int J Mol Sci. 2016;17:12.
  • Engen PA, Green SJ, Voigt RM, et al. The gastrointestinal microbiome: alcohol effects on the composition of intestinal microbiota. Alcohol Res. 2015;37(2):223–236.
  • Thaiss CA, Zeevi D, Levy M, et al. Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell. 2014;159(3):514–529.
  • Thaiss CA, Levy M, Korem T, et al. Microbiota diurnal rhythmicity programs host transcriptome oscillations. Cell. 2016;167(6):1495–1510.
  • Voigt RM, Forsyth CB, Green SJ, et al. Circadian disorganization alters intestinal microbiota. PLoS One. 2014;9(5):e97500.
  • Voigt RM, Summa KC, Forsyth CB, et al. The circadian clock mutation promotes intestinal dysbiosis. Alcohol Clin Exp Res. 2016;40(2):335–347.
  • Tahara Y, Yamazaki M, Sukigara H, et al. Gut microbiota-derived short chain fatty acids induce circadian clock entrainment in mouse peripheral tissue. Sci Rep. 2018;8(1):1395.
  • Huang YJ, Pai YC, Yu LC. Host-microbiota interaction and intestinal epithelial functions under circadian control: implications in colitis and metabolic disorders. Chin J Physiol. 2018;61(6):325–340.
  • Man K, Loudon A, Chawla A. Immunity around the clock. Science. 2016;354(6315):999–1003.
  • Labrecque N, Cermakian N. Circadian clocks in the immune system. J Biol Rhythms. 2015;30(4):277–290.
  • Scheiermann C, Kunisaki Y, Frenette PS. Circadian control of the immune system. Nat Rev Immunol. 2013;13(3):190–198.
  • Halberg F, Johnson EA, Brown BW, et al. Susceptibility rhythm to e Coli endotoxin and bioassay. Proc Soc Exp Biol Med. 1960;103:142–144.
  • Tsoumtsa LL, Torre C, Ghigo E. Circadian control of antibacterial immunity: findings from animal models. Front Cell Infect Microbiol. 2016;6:54.
  • Curtis AM, Fagundes CT, Yang G, et al. Circadian control of innate immunity in macrophages by mir-155 targeting bmal1. Proc Natl Acad Sci U S A. 2015;112(23):7231–7236.
  • Nguyen KD, Fentress SJ, Qiu Y, et al. Circadian gene bmal1 regulates diurnal oscillations of ly6c(hi) inflammatory monocytes. Science. 2013;341(6153):1483–1488.
  • Liu J, Malkani G, Shi X, et al. The circadian clock period 2 gene regulates gamma interferon production of nk cells in host response to lipopolysaccharide-induced endotoxic shock. Infect Immun. 2006;74(8):4750–4756.
  • Scheiermann C, Kunisaki Y, Lucas D, et al. Adrenergic nerves govern circadian leukocyte recruitment to tissues. Immunity. 2012;37(2):290–301.
  • Silver AC, Arjona A, Walker WE, et al. The circadian clock controls toll-like receptor 9-mediated innate and adaptive immunity. Immunity. 2012;36(2):251–261.
  • Feigin RD, San Joaquin VH, Haymond MW, et al. Daily periodicity of susceptibility of mice to pneumococcal infection. Nature. 1969;224(5217):379–380.
  • Castanon-Cervantes O, Wu M, Ehlen JC, et al. Dysregulation of inflammatory responses by chronic circadian disruption. J Immunol. 2010;185(10):5796–5805.
  • Born J, Lange T, Hansen K, et al. Effects of sleep and circadian rhythm on human circulating immune cells. J Immunol. 1997;158(9):4454–4464.
  • Curtis AM, Bellet MM, Sassone-Corsi P, et al. Circadian clock proteins and immunity. Immunity. 2014;40(2):178–186.
  • Johnston JD, Ordovas JM, Scheer FA, et al. Circadian rhythms, metabolism, and chrononutrition in rodents and humans. Adv Nutr. 2016;7(2):399–406.
  • Dibner C, Schibler U. Circadian timing of metabolism in animal models and humans. J Intern Med. 2015;277(5):513–527.
  • Perelis M, Ramsey KM, Bass J. The molecular clock as a metabolic rheostat. Diabetes Obes Metab. 2015;17(Suppl 1):99–105.
  • Depner CM, Stothard ER, Wright KP Jr. Metabolic consequences of sleep and circadian disorders. Curr Diab Rep. 2014;14(7):507.
  • Markwald RR, Melanson EL, Smith MR, et al. Impact of insufficient sleep on total daily energy expenditure, food intake, and weight gain. Proc Natl Acad Sci USA. 2013;110(14):5695–5700.
  • Nguyen J, Wright KP Jr. Influence of weeks of circadian misalignment on leptin levels. Nat Sci Sleep. 2010;2:9–18.
  • Spiegel K, Tasali E, Leproult R, et al. Twenty-four-hour profiles of acylated and total ghrelin: relationship with glucose levels and impact of time of day and sleep. J Clin Endocrinol Metab. 2011;96(2):486–493.
  • Van Cauter E, Polonsky KS, Scheen AJ. Roles of circadian rhythmicity and sleep in human glucose regulation. Endocr Rev. 1997;18(5):716–738.
  • Scheer FA, Hilton MF, Mantzoros CS, et al. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc Natl Acad Sci USA. 2009;106(11):4453–4458.
  • Karlsson B, Knutsson A, Lindahl B. Is there an association between shift work and having a metabolic syndrome? Results from a population based study of 27,485 people. Occup Environ Med. 2001;58(11):747–752.
  • Antunes LC, Levandovski R, Dantas G, et al. Obesity and shift work: chronobiological aspects. Nutr Res Rev. 2010;23(1):155–168.
  • Li Y, Sato Y, Yamaguchi N. Shift work and the risk of metabolic syndrome: a nested case-control study. Int J Occup Environ Health. 2011;17(2):154–160.
  • Knutson KL, Spiegel K, Penev P, et al. The metabolic consequences of sleep deprivation Sleep. Med Rev. 2007;11(3):163–178.
  • Buxton OM, Cain SW, O’Connor SP, et al. Adverse metabolic consequences in humans of prolonged sleep restriction combined with circadian disruption. Sci Transl Med. 2012;4(129):129ra43.
  • Bouatia-Naji N, Bonnefond A, Cavalcanti-Proenca C, et al. A variant near mtnr1b is associated with increased fasting plasma glucose levels and type 2 diabetes risk. Nat Genet. 2009;41(1):89–94.
  • Prokopenko I, Langenberg C, Florez JC, et al. Variants in mtnr1b influence fasting glucose levels. Nat Genet. 2009;41(1):77–81.
  • Radziuk J, Pye S. Diurnal rhythm in endogenous glucose production is a major contributor to fasting hyperglycaemia in type 2 diabetes. Suprachiasmatic deficit or limit cycle behaviour? Diabetologia. 2006;49(7):1619–1628.
  • Arble DM, Bass J, Laposky AD, et al. Circadian timing of food intake contributes to weight gain. Obesity (Silver Spring). 2009;17(11):2100–2102.
  • Leproult R, Holmback U, Van CE. Circadian misalignment augments markers of insulin resistance and inflammation, independently of sleep loss. Diabetes. 2014;63(6):1860–1869.
  • Zaidi D, Wine E. An update on travelers’ diarrhea Curr. Opin Gastroenterol. 2015;31(1):7–13.
  • Logan RW, Sarkar DK. Circadian nature of immune function. Mol Cell Endocrinol. 2012;349(1):82–90.
  • Keller M, Mazuch J, Abraham U, et al. A circadian clock in macrophages controls inflammatory immune responses. Proc Natl Acad Sci USA. 2009;106(50):21407–21412.
  • Narasimamurthy R, Hatori M, Nayak SK, et al. Circadian clock protein cryptochrome regulates the expression of proinflammatory cytokines. Proc Natl Acad Sci USA. 2012;109(31):12662–12667.
  • Wongwiwat M, Sukapanit S, Triyanond C, et al. Circadian rhythm of the resistance of mice to acute pneumococcal infection. Infect Immun. 1972;5(4):442–448.
  • Bellet MM, Deriu E, Liu JZ, et al. Circadian clock regulates the host response to salmonella. Proc Natl Acad Sci USA. 2013;110(24):9897–9902.
  • Hriscu M, Saulea G, Ostriceanu S, et al. Circadian phagocytic activity in rats under light-dark and constant light regimens. Rom J Physiol. 2002;39–40:17–26.
  • Spengler ML, Kuropatwinski KK, Comas M, et al. Core circadian protein clock is a positive regulator of nf-kappab-mediated transcription. Proc Natl Acad Sci USA. 2012;109(37):E2457–E65.
  • Yu X, Rollins D, Ruhn KA, et al. Th17 cell differentiation is regulated by the circadian clock. Science. 2013;342(6159):727–730.
  • Segawa K, Nakazawa S, Tsukamoto Y, et al. Peptic ulcer is prevalent among shift workers. Digestive Dis Sci. 1987;32(5):449–453.
  • Lin HY, Weng SF, Lin HJ, et al. Peptic ulcer disease in healthcare workers: a nationwide population-based cohort study. PLoS One. 2015;10(8):e0135456.
  • Pietroiusti A, Forlini A, Magrini A, et al. Shift work increases the frequency of duodenal ulcer in h pylori infected workers. Occup Environ Med. 2006;63(11):773–775.
  • Jones MP. The role of psychosocial factors in peptic ulcer disease: beyond helicobacter pylori and nsaids. J Psychosom Res. 2006;60(4):407–412.
  • Konturek SJ, Bielanski W, Plonka M, et al. Helicobacter pylori, non-steroidal anti-inflammatory drugs and smoking in risk pattern of gastroduodenal ulcers. Scand J Gastroenterol. 2003;38(9):923–930.
  • Tarquini B, Cecchettin M, Cariddi A. Serum gastrin and pepsinogen in shift workers Int Arch. Occup Environ Health. 1986;58(2):99–103.
  • Johns CE, Newton JL, Westley BR, et al. The diurnal rhythm of the cytoprotective human trefoil protein tff2 is reduced by factors associated with gastric mucosal damage: ageing, helicobacter pylori infection, and sleep deprivation. Am J Gastroenterol. 2005;100(7):1491–1497.
  • Semple JI, Newton JL, Westley BR, et al. Dramatic diurnal variation in the concentration of the human trefoil peptide tff2 in gastric juice. Gut. 2001;48(5):648–655.
  • Zober A, Schilling D, Ott MG, et al. Helicobacter pylori infection: prevalence and clinical relevance in a large company. J Occup Environ Med. 1998;40(7):586–594.
  • van MA, Spallek M, Groneberg DA, et al. Correlates shift work with increased risk of gastrointestinal complaints or frequency of gastritis or peptic ulcer in h. Pylori-infected shift workers? Int Arch Occup Environ Health. 2010;83(4):423–431.
  • Peters MN, Richardson CT. Stressful life events, acid hypersecretion, and ulcer disease. Gastroenterology. 1983;84(1):114–119.
  • Moore JG, Larsen KR, Barattini P, et al. Asynchrony in circadian rhythms of gastric function in the rat. A model for gastric mucosal injury. Digestive Dis Sci. 1994;39(8):1619–1624.
  • Iwakura N, Fujiwara Y, Shiba M, et al. Characteristics of sleep disturbances in patients with gastroesophageal reflux disease. Intern Med. 2016;55(12):1511–1517.
  • Moore JG, Merki H. Gastrointestinal tract. In: Redfern PH, Lemmer B, editors. Physilogy and pharmacology of biological rhythms. Handbook of experimental pharmacology. Vol. 125. Berlin, Heidelberg: Springer; 1997. p. 351–373.
  • Chung TH, Lee J, Kim MC. Impact of night-shift work on the prevalence of erosive esophagitis in shipyard male workers. Int Arch Occup Environ Health. 2016;89(6):961–966.
  • Li YM, Du J, Zhang H, et al. Epidemiological investigation in outpatients with symptomatic gastroesophageal reflux from the department of medicine in Zhejiang Province, East China. J Gastroenterol Hepatol. 2008;23(2):283–289.
  • Yang SC, Chen CL, Yi CH, et al. Changes in gene expression patterns of circadian-clock, transient receptor potential vanilloid-1 and nerve growth factor in inflamed human esophagus. Sci Rep. 2015;5:13602.
  • Konturek SJ, Konturek PC, Brzozowska I, et al. Localization and biological activities of melatonin in intact and diseased gastrointestinal tract (git). J Physiol Pharmacol. 2007;58(3):381–405.
  • Ananthakrishnan AN, Long MD, Martin CF, et al. Sleep disturbance and risk of active disease in patients with Crohn’s disease and ulcerative colitis. Clin Gastroenterol Hepatol. 2013;11(8):965–971.
  • Ballou S, Alhassan E, Hon E, et al. Sleep disturbances are commonly reported among patients presenting to a gastroenterology clinic. Digestive Dis Sci. 2018.
  • Zingone F, Siniscalchi M, Capone P, et al. The quality of sleep in patients with coeliac disease Aliment. Pharmacol Ther. 2010;32(8):1031–1036.
  • Marild K, Morgenthaler TI, Somers VK, et al. Increased use of hypnotics in individuals with celiac disease: a nationwide case-control study BMC. Gastroenterol. 2015;15:10.
  • Ali T, Madhoun MF, Orr WC, et al. Assessment of the relationship between quality of sleep and disease activity in inflammatory bowel disease patients. Inflamm Bowel Dis. 2013;19(11):2440–2443.
  • Preuss F, Tang Y, Laposky AD, et al. Adverse effects of chronic circadian desynchronization in animals in a “challenging” environment. Am J Physiol Regul Integr Comp Physiol. 2008;295(6):R2034–R40.
  • Boggild H, Tuchsen F, Orhede E. Occupation employment status and chronic inflammatory bowel disease in denmark. Int J Epidemiol. 1996;25(3):630–637.
  • Mazzoccoli G, Palmieri O, Corritore G, et al. Association study of a polymorphism in clock gene period3 and risk of inflammatory bowel disease. Chronobiol Int. 2012;29(8):994–1003.
  • Burgess HJ, Swanson GR, Keshavarzian A. Endogenous melatonin profiles in asymptomatic inflammatory bowel disease. Scand J Gastroenterol. 2010;45(6):759–761.
  • Chakradeo PS, Keshavarzian A, Singh S, et al. Chronotype, social jet lag, sleep debt and food timing in inflammatory bowel disease. Sleep Med. 2018;52:188–195.
  • Chrobak AA, Nowakowski J, Zwolinska-Wcislo M, et al. Associations between chronotype, sleep disturbances and seasonality with fatigue and inflammatory bowel disease symptoms. Chronobiol Int. 2018;1–11.
  • Mazzoccoli G, Vinciguerra M, Papa G, et al. Circadian clock circuitry in colorectal cancer world. J Gastroenterol. 2014;20(15):4197–4207.
  • Masri S, Kinouchi K, Sassone-Corsi P. Circadian clocks, epigenetics, and cancer. Curr Opin Oncol. 2015;27(1):50–56.
  • Zeng ZL, Wu MW, Sun J, et al. Effects of the biological clock gene bmal1 on tumour growth and anti-cancer drug activity. J Biochem. 2010;148(3):319–326.
  • Yang X, Wood PA, Ansell C, et al. Circadian time-dependent tumor suppressor function of period genes. Integr Cancer Ther. 2009;8(4):309–316.
  • Wood PA, Yang X, Hrushesky WJ. Clock genes and cancer. Integr Cancer Ther. 2009;8(4):303–308.
  • Mazzoccoli G, Panza A, Valvano MR, et al. Clock gene expression levels and relationship with clinical and pathological features in colorectal cancer patients. Chronobiol Int. 2011;28(10):841–851.
  • Mostafaie N, Kallay E, Sauerzapf E, et al. Correlated downregulation of estrogen receptor beta and the circadian clock gene per1 in human colorectal cancer. Mol Carcinog. 2009;48(7):642–647.
  • Alhopuro P, Bjorklund M, Sammalkorpi H, et al. Mutations in the circadian gene clock in colorectal cancer. Mol Cancer Res. 2010;8(7):952–960.
  • Wang Y, Hua L, Lu C, et al. Expression of circadian clock gene human period2 (hper2) in human colorectal carcinoma. World J Surg Oncol. 2011;9:166.
  • Wang X, Yan D, Teng M, et al. Reduced expression of per3 is associated with incidence and development of colon cancer. Ann Surg Oncol. 2012;19(9):3081–3088.
  • Schernhammer ES, Laden F, Speizer FE, et al. Night-shift work and risk of colorectal cancer in the nurses’ health study. J Natl Cancer Inst. 2003;95(11):825–828.
  • Wang X, Ji A, Zhu Y, et al. A meta-analysis including dose-response relationship between night shift work and the risk of colorectal cancer. Oncotarget. 2015;6(28):25046–25060.
  • Fine L. Sleep: important considerations in management of pain. Phys Med Rehabil Clin N Am. 2015;26(2):301–308.
  • Tavano F, Pazienza V, Fontana A, et al. Sirt1 and circadian gene expression in pancreatic ductal adenocarcinoma: effect of starvation. Chronobiol Int. 2015;32(4):497–512.
  • Smolensky MH, Portaluppi F, Manfredini R, et al. Diurnal and twenty-four hour patterning of human diseases: acute and chronic common and uncommon medical conditions. Sleep Med Rev. 2015;21:12–22.
  • Yu JH, Yun CH, Ahn JH, et al. Evening chronotype is associated with metabolic disorders and body composition in middle-aged adults. J Clin Endocrinol Metab. 2015;100(4):1494–1502.
  • Arora T, Taheri S. Associations among late chronotype, body mass index and dietary behaviors in young adolescents. Int J Obes (Lond). 2015;39(1):39–44.
  • Asher G, Sassone-Corsi P. Time for food: the intimate interplay between nutrition, metabolism, and the circadian clock. Cell. 2015;161(1):84–92.
  • Jiang P, Turek FW. The endogenous circadian clock programs animals to eat at certain times of the 24-hour day: what if we ignore the clock? Physiol Behav. 2018;193(Pt B):211–217.
  • Jakubowicz D, Barnea M, Wainstein J, et al. High caloric intake at breakfast vs. Dinner differentially influences weight loss of overweight and obese women. Obesity (Silver Spring). 2013;21(12):2504–2512.
  • Garaulet M, Gomez-Abellan P, Alburquerque-Bejar JJ, et al. Timing of food intake predicts weight loss effectiveness. Int J Obes Lond. 2013;37(4):604–611.
  • Ruiz-Lozano T, Vidal J, de Hollanda A, et al. Timing of food intake is associated with weight loss evolution in severe obese patients after bariatric surgery. Clin Nutr. 2016;35(6):1308–1314.
  • Salgado-Delgado R, Angeles-Castellanos M, Saderi N, et al. Food intake during the normal activity phase prevents obesity and circadian desynchrony in a rat model of night work. Endocrinology. 2010;151(3):1019–1029.
  • Ferrannini E, Ramos SJ, Salsali A, et al. Dapagliflozin monotherapy in type 2 diabetic patients with inadequate glycemic control by diet and exercise: a randomized, double-blind, placebo-controlled, phase 3 trial. Diabetes Care. 2010;33(10):2217–2224.
  • Mure LS, Le HD, Benegiamo G, et al. Diurnal transcriptome atlas of a primate across major neural and peripheral tissues. Science. 2018;359(6381).
  • Levi F, Zidani R, Misset JL. Randomised multicentre trial of chronotherapy with oxaliplatin, fluorouracil, and folinic acid in metastatic colorectal cancer. Int Organ Cancer Chronotherapy Lancet. 1997;350(9079):681–686.
  • Wei K, Wang Q, Gan J, et al. Mapping genes for drug chronotherapy. Drug Discov Today. 2018;23(11):1883–1888.
  • Esteban-Zubero E, Lopez-Pingarron L, Alatorre-Jimenez MA, et al. Melatonin’s role as a co-adjuvant treatment in colonic diseases A review. Life Sci. 2017;170:72–81.
  • Erren TC, Reiter RJ. Light hygiene: time to make preventive use of insights – old and new – into the nexus of the drug light, melatonin, clocks, chronodisruption and public health. Med Hypotheses. 2009;73(4):537–541.
  • Berry J, Bumpers K, Ogunlade V, et al. Examining racial disparities in colorectal cancer care. J Psychosoc Oncol. 2009;27(1):59–83.
  • Dimou A, Syrigos KN, Saif MW. Disparities in colorectal cancer in african-americans vs whites: before and after diagnosis. World J Gastroenterol. 2009;15(30):3734–3743.
  • Riestra P, Gebreab SY, Xu R, et al. Circadian clock gene polymorphisms in relation to sleep patterns and obesity in African Americans: findings from the Jackson Heart Study. BMC Genet. 2017;18(1):58.
  • Eastman CI, Suh C, Tomaka VA, et al. Circadian rhythm phase shifts and endogenous free-running circadian period differ between African-Americans and European-Americans. Sci Rep. 2015;5:8381.
  • Paech GM, Crowley SJ, Fogg LF, et al. Advancing the sleep/wake schedule impacts the sleep of African-Americans more than European-Americans. PLoS One. 2017;12(10):e0186887.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.