Abstract
The importance of circadian rhythm has been established through its evolutionary conservation and its connection to many health conditions. Circadian deregulation has emerged as an important risk factor for metabolic disruption and related chronic diseases. Chronic diseases are on the rise worldwide, and emerging evidence points toward restoration of circadian rhythms as a propitious approach to preventing and improving prognosis of many chronic disorders. This review will outline the evidence supporting the importance of the circadian system in metabolism by debriefing the molecular basis for the interaction between circadian timing and metabolic health and behavioral, genetic, and human epidemiological studies indicating the health implications of chrono-disruption.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Ward BW, Schiller JS, Goodman RA (2014) Multiple chronic conditions among US adults: a 2012 update. Prev Chronic Dis 11:E62
Reynolds K, He J (2005) Epidemiology of the metabolic syndrome. Am J Med Sci 330:273–279
Grundy SM, Brewer HB Jr, Cleeman JI, Smith SC Jr, Lenfant C (2004) Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Arterioscler Thromb Vasc Biol 24:e13–e18
Vita-Finzi L (2005) Preventing chronic diseases: a vital investment. World Health Organization, Geneva
Cordain L, Eaton S, Brand Miller J, Mann N, Hill K (2002) Original communications-the paradoxical nature of hunter-gatherer diets: meat-based, yet non-atherogenic. Eur J Clin Nutr 56:S42
Hardin PE, Panda S (2013) Circadian timekeeping and output mechanisms in animals. Curr Opin Neurobiol 23:724–731
Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, Albrecht U, Schibler U (2002) The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110:251–260
Sato TK, Panda S, Miraglia LJ, Reyes TM, Rudic RD, McNamara P, Naik KA, FitzGerald GA, Kay SA, Hogenesch JB (2004) A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron 43:527–537
Hughes M, Deharo L, Pulivarthy SR, Gu J, Hayes K, Panda S, Hogenesch JB (2007) High-resolution time course analysis of gene expression from pituitary. Cold Spring Harb Symp Quant Biol 72:381–386
Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307–320
Zhang R, Lahens NF, Ballance HI, Hughes ME, Hogenesch JB (2014) A circadian gene expression atlas in mammals: implications for biology and medicine. Proc Natl Acad Sci U S A 111:16219–16224
Nayak SK, Jegla T, Panda S (2007) Role of a novel photopigment, melanopsin, in behavioral adaptation to light. Cell Mol Life Sci 64:144–154
Aton SJ, Herzog ED (2005) Come together, right…now: synchronization of rhythms in a mammalian circadian clock. Neuron 48:531–534
Mohawk JA, Green CB, Takahashi JS (2012) Central and peripheral circadian clocks in mammals. Annu Rev Neurosci 35:445–462
Welsh DK, Yoo SH, Liu AC, Takahashi JS, Kay SA (2004) Bioluminescence imaging of individual fibroblasts reveals persistent, independently phased circadian rhythms of clock gene expression. Curr Biol 14:2289–2295
Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M, Block GD, Sakaki Y, Menaker M, Tei H (2000) Resetting central and peripheral circadian oscillators in transgenic rats. Science 288:682–685
Hughes ME, Hong HK, Chong JL, Indacochea AA, Lee SS, Han M, Takahashi JS, Hogenesch JB (2012) Brain-specific rescue of clock reveals system-driven transcriptional rhythms in peripheral tissue. PLoS Genet 8:e1002835
Kornmann B, Schaad O, Bujard H, Takahashi JS, Schibler U (2007a) System-driven and oscillator-dependent circadian transcription in mice with a conditionally active liver clock. PLoS Biol 5:e34
Kornmann B, Schaad O, Reinke H, Saini C, Schibler U (2007b) Regulation of circadian gene expression in liver by systemic signals and hepatocyte oscillators. In: Cold Spring Harbor symposia on quantitative biology. Cold Spring Harbor Laboratory Press, pp 319–330
Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, Reichardt HM, Schutz G, Schibler U (2000) Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289:2344–2347
Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, Schibler U (2000) Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 14:2950–2961
Vollmers C, Gill S, DiTacchio L, Pulivarthy SR, Le HD, Panda S (2009) Time of feeding and the intrinsic circadian clock drive rhythms in hepatic gene expression. Proc Natl Acad Sci U S A 106:21453–21458
Asher G, Sassone-Corsi P (2015) Time for food: the intimate interplay between nutrition, metabolism, and the circadian clock. Cell 161:84–92
Gachon F, Olela FF, Schaad O, Descombes P, Schibler U (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
Lamia KA, Storch KF, Weitz CJ (2008) Physiological significance of a peripheral tissue circadian clock. Proc Natl Acad Sci U S A 105:15172–15177
Rudic RD, McNamara P, Curtis AM, Boston RC, Panda S, Hogenesch JB, Fitzgerald GA (2004) BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biol 2:e377
Inoki K, Kim J, Guan KL (2011) AMPK and mTOR in cellular energy homeostasis and drug targets. Annu Rev Pharmacol Toxicol 52(1):381–400
Lamia KA, Sachdeva UM, DiTacchio L, Williams EC, Alvarez JG, Egan DF, Vasquez DS, Juguilon H, Panda S, Shaw RJ, Thompson CB, Evans RM (2009) AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science 326:437–440
Altarejos JY, Montminy M (2011) CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat Rev Mol Cell Biol 12:141–151
Hatori M, Panda S (2010) CRY links the circadian clock and CREB-mediated gluconeogenesis. Cell Res 20:1285–1288
Guillaumond F, Gréchez-Cassiau A, Subramaniam M, Brangolo S, Peteri-Brünback B, Staels B, Fiévet C, Spelsberg TC, Delaunay F, Teboul M (2010) Krüppel-like factor KLF10 is a link between the circadian clock and metabolism in liver. Mol Cell Biol 30:3059–3070
Nakahata Y, Sahar S, Astarita G, Kaluzova M, Sassone-Corsi P (2009) Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science 324:654–657
Ramsey KM, Yoshino J, Brace CS, Abrassart D, Kobayashi Y, Marcheva B, Hong HK, Chong JL, Buhr ED, Lee C, Takahashi JS, Imai S, Bass J (2009) Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science 324:651–654
Burkle A (2001) Physiology and pathophysiology of poly(ADP-ribosyl)ation. Bioessays 23:795–806
Asher G, Reinke H, Altmeyer M, Gutierrez-Arcelus M, Hottiger MO, Schibler U (2010) Poly(ADP-ribose) polymerase 1 participates in the phase entrainment of circadian clocks to feeding. Cell 142:943–953
Dentin R, Liu Y, Koo SH, Hedrick S, Vargas T, Heredia J, Yates J 3rd, Montminy M (2007) Insulin modulates gluconeogenesis by inhibition of the coactivator TORC2. Nature 449:366–369
Puigserver P, Rhee J, Donovan J, Walkey CJ, Yoon JC, Oriente F, Kitamura Y, Altomonte J, Dong H, Accili D, Spiegelman BM (2003) Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1alpha interaction. Nature 423:550–555
Zhang W, Patil S, Chauhan B, Guo S, Powell DR, Le J, Klotsas A, Matika R, Xiao X, Franks R, Heidenreich KA, Sajan MP, Farese RV, Stolz DB, Tso P, Koo SH, Montminy M, Unterman TG (2006) FoxO1 regulates multiple metabolic pathways in the liver: effects on gluconeogenic, glycolytic, and lipogenic gene expression. J Biol Chem 281:10105–10117
Espenshade PJ, Hughes AL (2007) Regulation of sterol synthesis in eukaryotes. Annu Rev Genet 41:401–427
Bheda P, Jing H, Wolberger C, Lin H (2016) The substrate specificity of sirtuins. Ann Rev Biochem 85:405–429
Sahar S, Sassone-Corsi P (2009) Metabolism and cancer: the circadian clock connection. Nat Rev Cancer 9:886–896
Yang X, Downes M, Yu RT, Bookout AL, He W, Straume M, Mangelsdorf DJ, Evans RM (2006) Nuclear receptor expression links the circadian clock to metabolism. Cell 126:801–810
Bugge A, Feng D, Everett LJ, Briggs ER, Mullican SE, Wang F, Jager J, Lazar MA (2012) Rev-erbalpha and Rev-erbbeta coordinately protect the circadian clock and normal metabolic function. Genes Dev 26:657–667
Cho H, Zhao X, Hatori M, Yu RT, Barish GD, Lam MT, Chong LW, DiTacchio L, Atkins AR, Glass CK, Liddle C, Auwerx J, Downes M, Panda S, Evans RM (2012) Regulation of circadian behaviour and metabolism by REV-ERB-alpha and REV-ERB-beta. Nature 485:123–127
Gerhart-Hines Z, Feng D, Emmett MJ, Everett LJ, Loro E, Briggs ER, Bugge A, Hou C, Ferrara C, Seale P, Pryma DA, Khurana TS, Lazar MA (2013) The nuclear receptor Rev-erbalpha controls circadian thermogenic plasticity. Nature 503:410–413
Fang B, Lazar MA (2015) Dissecting the Rev-erbalpha cistrome and the mechanisms controlling circadian transcription in liver. Cold Spring Harb Symp Quant Biol 80:233–238
Eckel-Mahan K, Sassone-Corsi P (2013) Metabolism and the circadian clock converge. Physiol Rev 93:107–135
Eckel-Mahan KL, Patel VR, de Mateo S, Orozco-Solis R, Ceglia NJ, Sahar S, Dilag-Penilla SA, Dyar KA, Baldi P, Sassone-Corsi P (2013) Reprogramming of the circadian clock by nutritional challenge. Cell 155:1464–1478
Mokdad AH, Marks JS, Stroup DF, Gerberding JL (2004) Actual causes of death in the United States, 2000. JAMA 291:1238–1245
Bass J, Takahashi JS (2010) Circadian integration of metabolism and energetics. Science 330:1349–1354
Zarrinpar A, Chaix A, Panda S (2016) Daily eating patterns and their impact on health and disease. Trends Endocrinol Metab 27:69–83
Lamia KA, Papp SJ, Yu RT, Barish GD, Uhlenhaut NH, Jonker JW, Downes M, Evans RM (2011) Cryptochromes mediate rhythmic repression of the glucocorticoid receptor. Nature 480:552–556
Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, McDearmon E, Laposky A, Losee-Olson S, Easton A, Jensen DR, Eckel RH, Takahashi JS, Bass J (2005) Obesity and metabolic syndrome in circadian clock mutant mice. Science 308:1043–1045
Paschos GK, Ibrahim S, Song WL, Kunieda T, Grant G, Reyes TM, Bradfield CA, Vaughan CH, Eiden M, Masoodi M, Griffin JL, Wang F, Lawson JA, Fitzgerald GA (2012) Obesity in mice with adipocyte-specific deletion of clock component Arntl. Nat Med 18:1768–1777
Castanon-Cervantes O, Wu M, Ehlen JC, Paul K, Gamble KL, Johnson RL, Besing RC, Menaker M, Gewirtz AT, Davidson AJ (2010) Dysregulation of inflammatory responses by chronic circadian disruption. J Immunol 185:5796–5805
Marpegán L, Bekinschtein TA, Costas MA, Golombek DA (2005) Circadian responses to endotoxin treatment in mice. J Neuroimmunol 160:102–109
Redwine L, Hauger RL, Gillin JC, Irwin M (2000) Effects of sleep and sleep deprivation on interleukin-6, growth hormone, cortisol, and melatonin levels in Humans 1. J Clin Endocrinol Metabol 85:3597–3603
Boucher H, Vanneaux V, Domet T, Parouchev A, Larghero J (2016) Circadian clock genes modulate human bone marrow mesenchymal stem cell differentiation, migration and cell cycle. PLoS One 11:e0146674
Christensen J, Agger K, Cloos PA, Pasini D, Rose S, Sennels L, Rappsilber J, Hansen KH, Salcini AE, Helin K (2007) RBP2 belongs to a family of demethylases, specific for tri-and dimethylated lysine 4 on histone 3. Cell 128:1063–1076
DiTacchio L, Le HD, Vollmers C, Hatori M, Witcher M, Secombe J, Panda S (2011) Histone lysine demethylase JARID1a activates CLOCK-BMAL1 and influences the circadian clock. Science 333:1881–1885
Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ, Cua DJ, Littman DR (2006) The orphan nuclear receptor RORγt directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126:1121–1133
Narasimamurthy R, Hatori M, Nayak SK, Liu F, Panda S, Verma IM (2012) Circadian clock protein cryptochrome regulates the expression of proinflammatory cytokines. Proc Natl Acad Sci U S A 109:12662–12667
Keller M, Mazuch J, Abraham U, Eom GD, Herzog ED, Volk H-D, Kramer A, Maier B (2009) A circadian clock in macrophages controls inflammatory immune responses. Proc Natl Acad Sci 106:21407–21412
Durgan DJ, Young ME (2010) The cardiomyocyte circadian clock: emerging roles in health and disease. Circ Res 106:647–658
Bray MS, Shaw CA, Moore MW, Garcia RA, Zanquetta MM, Durgan DJ, Jeong WJ, Tsai JY, Bugger H, Zhang D, Rohrwasser A, Rennison JH, Dyck JR, Litwin SE, Hardin PE, Chow CW, Chandler MP, Abel ED, Young ME (2008) Disruption of the circadian clock within the cardiomyocyte influences myocardial contractile function, metabolism, and gene expression. Am J Physiol Heart Circ Physiol 294:H1036–H1047
Tsai JY, Kienesberger PC, Pulinilkunnil T, Sailors MH, Durgan DJ, Villegas-Montoya C, Jahoor A, Gonzalez R, Garvey ME, Boland B, Blasier Z, McElfresh TA, Nannegari V, Chow CW, Heird WC, Chandler MP, Dyck JR, Bray MS, Young ME (2010) Direct regulation of myocardial triglyceride metabolism by the cardiomyocyte circadian clock. J Biol Chem 285:2918–2929
Young ME, Brewer RA, Peliciari-Garcia RA, Collins HE, He L, Birky TL, Peden BW, Thompson EG, Ammons BJ, Bray MS, Chatham JC, Wende AR, Yang Q, Chow CW, Martino TA, Gamble KL (2014) Cardiomyocyte-specific BMAL1 plays critical roles in metabolism, signaling, and maintenance of contractile function of the heart. J Biol Rhythms 29:257–276
Young ME, Razeghi P, Cedars AM, Guthrie PH, Taegtmeyer H (2001) Intrinsic diurnal variations in cardiac metabolism and contractile function. Circ Res 89:1199–1208
Young ME, Razeghi P, Taegtmeyer H (2001) Clock genes in the heart: characterization and attenuation with hypertrophy. Circ Res 88:1142–1150
Reiter RJ, Calvo JR, Karbownik M, Qi W, Tan DX (2000) Melatonin and its relation to the immune system and inflammation. Ann N Y Acad Sci 917:376–386
Sahna E, Parlakpinar H, Turkoz Y, Acet A (2005) Protective effects of melatonin on myocardial ischemia-reperfusion induced infarct size and oxidative changes. Physiol Res 54:491
Jeyaraj D, Haldar SM, Wan X, McCauley MD, Ripperger JA, Hu K, Lu Y, Eapen BL, Sharma N, Ficker E, Cutler MJ, Gulick J, Sanbe A, Robbins J, Demolombe S, Kondratov RV, Shea SA, Albrecht U, Wehrens XH, Rosenbaum DS, Jain MK (2012) Circadian rhythms govern cardiac repolarization and arrhythmogenesis. Nature 483:96–99
Stevens RG, Hansen J, Costa G, Haus E, Kauppinen T, Aronson KJ, Castaño-Vinyals G, Davis S, Frings-Dresen MH, Fritschi L, Kogevinas M, Kogi K, Lie JA, Lowden A, Peplonska B, Pesch B, Pukkala E, Schernhammer E, Travis RC, Vermeulen R, Zheng T, Cogliano V, Straif K (2011) Considerations of circadian impact for defining ‘shift work’in cancer studies: IARC working group report. Occup Environ Med 68:154–162
Fu L, Lee CC (2003) The circadian clock: pacemaker and tumour suppressor. Nat Rev Cancer 3:350–361
Savvidis C, Koutsilieris M (2012) Circadian rhythm disruption in cancer biology. Mol Med 18:1249–1260
Matsuo T, Yamaguchi S, Mitsui S, Emi A, Shimoda F, Okamura H (2003) Control mechanism of the circadian clock for timing of cell division in vivo. Science 302:255–259, Epub 2003 Aug 2021
Chen S-T, Choo K-B, Hou M-F, Yeh K-T, Kuo S-J, Chang J-G (2005) Deregulated expression of the PER1, PER2 and PER3 genes in breast cancers. Carcinogenesis 26:1241–1246
Gery S, Komatsu N, Baldjyan L, Yu A, Koo D, Koeffler HP (2006) The circadian gene per1 plays an important role in cell growth and DNA damage control in human cancer cells. Mol Cell 22:375–382
Papp SJ, Huber A-L, Jordan SD, Kriebs A, Nguyen M, Moresco JJ, Yates JR, Lamia KA (2015) DNA damage shifts circadian clock time via Hausp-dependent Cry1 stabilization. Elife 4:e04883
Vander Heiden MG, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324:1029–1033
Ma D, Panda S, Lin JD (2011) Temporal orchestration of circadian autophagy rhythm by C/EBPbeta. EMBO J 30:4642–4651
Arble DM, Bass J, Behn CD, Butler MP, Challet E, Czeisler C, Depner CM, Elmquist J, Franken P, Grandner MA, Hanlon EC, Keene AC, Joyner MJ, Karatsoreos I, Kern PA, Klein S, Morris CJ, Pack AI, Panda S, Ptacek LJ, Punjabi NM, Sassone-Corsi P, Scheer FA, Saxena R, Seaquest ER, Thimgan MS, Van Cauter E, Wright KP (2015) Impact of sleep and circadian disruption on energy balance and diabetes: a summary of workshop discussions. Sleep 38:1849–1860
Qian J, Scheer FA (2016) Circadian system and glucose metabolism: implications for physiology and disease. Trends Endocrinol Metab 27:282–293
Fonken LK, Workman JL, Walton JC, Weil ZM, Morris JS, Haim A, Nelson RJ (2010) Light at night increases body mass by shifting the time of food intake. Proc Natl Acad Sci U S A 107:18664–18669
Adamovich Y, Rousso-Noori L, Zwighaft Z, Neufeld-Cohen A, Golik M, Kraut-Cohen J, Wang M, Han X, Asher G (2014) Circadian clocks and feeding time regulate the oscillations and levels of hepatic triglycerides. Cell Metab 19:319–330
Chaix A, Zarrinpar A, Miu P, Panda S (2014) Time-restricted feeding is a preventative and therapeutic intervention against diverse nutritional challenges. Cell Metab 20:991–1005
Hatori M, Vollmers C, Zarrinpar A, Ditacchio L, Bushong EA, Gill S, Leblanc M, Chaix A, Joens M, Fitzpatrick JA, Ellisman MH, Panda S (2012) Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab 15:848–860.
Liu Z, Huang M, Wu X, Shi G, Xing L, Dong Z, Qu Z, Yan J, Yang L, Panda S, Xu Y (2014) PER1 phosphorylation specifies feeding rhythm in mice. Cell Rep 7:1509–1520
Garaulet M, Gomez-Abellan P, Alburquerque-Bejar JJ, Lee YC, Ordovas JM, Scheer FA (2013) Timing of food intake predicts weight loss effectiveness. Int J Obes (Lond) 37:604–611
Gill S, Panda S (2015) A smartphone app reveals erratic diurnal eating patterns in humans that can be modulated for health benefits. Cell Metab 22:789–798
Marinac CR, Natarajan L, Sears DD, Gallo LC, Hartman SJ, Arredondo E, Patterson RE (2015) Prolonged nightly fasting and breast cancer risk: findings from NHANES (2009–2010). Cancer Epidemiol Biomarkers Prev: Publ Am Assoc Cancer Res Cosponsored Am Soc Prev Oncol 24:783–789
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer (India) Pvt. Ltd.
About this chapter
Cite this chapter
Sarkisian, B., Gupta, N.J., Panda, S. (2017). Circadian Regulation of Metabolism in Health and Diseases. In: Kumar, V. (eds) Biological Timekeeping: Clocks, Rhythms and Behaviour. Springer, New Delhi. https://doi.org/10.1007/978-81-322-3688-7_21
Download citation
DOI: https://doi.org/10.1007/978-81-322-3688-7_21
Published:
Publisher Name: Springer, New Delhi
Print ISBN: 978-81-322-3686-3
Online ISBN: 978-81-322-3688-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)