J Korean Diabetes.  2014 Dec;15(4):216-220. 10.4093/jkd.2014.15.4.216.

Circadian Rhythm Disruption and Metabolic Syndrome

• Kim D
• Jo YS

• KMID: 2173867
• DOI: http://doi.org/10.4093/jkd.2014.15.4.216

Abstract

Metabolic syndrome is a complex disorder and an emerging clinical challenge. It is induced by the interplay of genetic and environmental factors. Recently, evidence has emerged to suggest that circadian rhythm disruption is a new risk factor to explain the increased incidence of metabolic syndrome. This review summarizes circadian rhythm biology and the evidence linking circadian rhythm disruptions to metabolic syndrome, as related to lipid metabolism, glucose homeostasis, and cardiovascular function. Further understanding of circadian rhythm will aid the development of novel therapeutic strategies for metabolic syndrome.

Keyword

Circadian rhythm; Metabolic syndrome; Obesity; Diabetes mellitus; Cardiovascular disease

MeSH Terms

Biology
Cardiovascular Diseases
Circadian Rhythm*
Diabetes Mellitus
Glucose
Homeostasis
Incidence
Lipid Metabolism
Obesity
Risk Factors
Glucose

Figure

• 

  Fig. 1. Schematic summary of the core molecular clock related to circadian rhythm. Adapted from Sheikh-Ali M et al. Postgrad Med J 2014;90:461–6 [38].

Reference

References

1. Eckel RH, Alberti KG, Grundy SM, Zimmet PZ. The metabolic syndrome. Lancet. 2010; 375:181–3.

2. Park YW, Zhu S, Palaniappan L, Heshka S, Carnethon MR, Heymsfield SB. The metabolic syndrome: prevalence and associated risk factor findings in the US population from the Third National Health and Nutrition Examination Survey, 1988–1994. Arch Intern Med. 2003; 163:427–36.

3. Golombek DA, Casiraghi LP, Agostino PV, Paladino N, Duhart JM, Plano SA, Chiesa JJ. The times they're a-changing: effects of circadian desynchronization on physiology and disease. J Physiol Paris. 2013; 107:310–22.

4. Challet E. Circadian clocks, food intake, and metabolism. Prog Mol Biol Transl Sci. 2013; 119:105–35.

5. Dardente H, Cermakian N. Molecular circadian rhythms in central and peripheral clocks in mammals. Chronobiol Int. 2007; 24:195–213.

6. Ptitsyn AA, Zvonic S, Gimble JM. Digital signal processing reveals circadian baseline oscillation in majority of mammalian genes. PLoS Comput Biol. 2007; 3:e120.

7. Shimba S, Ishii N, Ohta Y, Ohno T, Watabe Y, Hayashi M, Wada T, Aoyagi T, Tezuka M. Brain and muscle Arnt-like protein-1 (BMAL1), a component of the molecular clock, regulates adipogenesis. Proc Natl Acad Sci U S A. 2005; 102:12071–6.

8. Shostak A, Meyer-Kovac J, Oster H. Circadian regulation of lipid mobilization in white adipose tissues. Diabetes. 2013; 62:2195–203.

9. 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. Obesity in mice with adipocyte-specific deletion of clock component Arntl. Nat Med. 2012; 18:1768–77.

10. Hussain MM, Pan X. Clock regulation of dietary lipid absorption. Curr Opin Clin Nutr Metab Care. 2012; 15:336–41.

11. Le Martelot G, Claudel T, Gatfield D, Schaad O, Kornmann B, Lo Sasso G, Moschetta A, Schibler U. REV-ERBalpha participates in circadian SREBP signaling and bile acid homeostasis. PLoS Biol. 2009; 7:e1000181.

12. Scott EM, Carter AM, Grant PJ. Association between polymorphisms in the Clock gene, obesity and the metabolic syndrome in man. Int J Obes (Lond). 2008; 32:658–62.

13. Garaulet M, Corbalán-Tutau MD, Madrid JA, Baraza JC, Parnell LD, Lee YC, Ordovas JM. PERIOD2 variants are associated with abdominal obesity, psycho-behavioral factors, and attrition in the dietary treatment of obesity. J Am Diet Assoc. 2010; 110:917–21.

14. Clements M, Berry G, Shi J, Ware S, Yates D, Johnson A. Projected mesothelioma incidence in men in New South Wales. Occup Environ Med. 2007; 64:747–52.

15. Karlsson BH, Knutsson AK, Lindahl BO, Alfredsson LS. Metabolic disturbances in male workers with rotating three-shift work. Results of the WOLF study. Int Arch Occup Environ Health. 2003; 76:424–30.

16. Ghiasvand M, Heshmat R, Golpira R, Haghpanah V, Soleimani A, Shoushtarizadeh P, Tavangar SM, Larijani B. Shift working and risk of lipid disorders: a cross-sectional study. Lipids Health Dis. 2006; 5:9.

17. Rudic RD, McNamara P, Curtis AM, Boston RC, Panda S, Hogenesch JB, Fitzgerald GA. BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biol. 2004; 2:e377.

18. Marcheva B, Ramsey KM, Buhr ED, Kobayashi Y, Su H, Ko CH, Ivanova G, Omura C, Mo S, Vitaterna MH, Lopez JP, Philipson LH, Bradfield CA, Crosby SD, JeBailey L, Wang X, Takahashi JS, Bass J. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature. 2010; 466:627–31.

19. 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. Obesity and metabolic syndrome in circadian Clock mutant mice. Science. 2005; 308:1043–5.

20. Lee J, Moulik M, Fang Z, Saha P, Zou F, Xu Y, Nelson DL, Ma K, Moore DD, Yechoor VK. Bmal1 and β-cell clock are required for adaptation to circadian disruption, and their loss of function leads to oxidative stress-induced β −cell failure in mice. Mol Cell Biol. 2013; 33:2327–38.

21. Lamia KA, Storch KF, Weitz CJ. Physiological significance of a peripheral tissue circadian clock. Proc Natl Acad Sci U S A. 2008; 105:15172–7.

22. Zhang EE, Liu Y, Dentin R, Pongsawakul PY, Liu AC, Hirota T, Nusinow DA, Sun X, Landais S, Kodama Y, Brenner DA, Montminy M, Kay SA. Cryptochrome mediates circadian regulation of cAMP signaling and hepatic gluconeogenesis. Nat Med. 2010; 16:1152–6.

23. Lamia KA, Papp SJ, Yu RT, Barish GD, Uhlenhaut NH, Jonker JW, Downes M, Evans RM. Cryptochromes mediate rhythmic repression of the glucocorticoid receptor. Nature. 2011; 480:552–6.

24. Englund A, Kovanen L, Saarikoski ST, Haukka J, Reunanen A, Aromaa A, Lönnqvist J, Partonen T. NPAS2 and PER2 are linked to risk factors of the metabolic syndrome. J Circadian Rhythms. 2009; 7:5.

25. Ando H, Takamura T, Matsuzawa-Nagata N, Shima KR, Eto T, Misu H, Shiramoto M, Tsuru T, Irie S, Fujimura A, Kaneko S. Clock gene expression in peripheral leucocytes of patients with type 2 diabetes. Diabetologia. 2009; 52:329–35.

26. Leproult R, Holmbäck U, Van Cauter E. Circadian misalignment augments markers of insulin resistance and inflammation, independently of sleep loss. Diabetes. 2014; 63:1860–9.

27. Durgan DJ, Young ME. The cardiomyocyte circadian clock: emerging roles in health and disease. Circ Res. 2010; 106:647–58.

28. Curtis AM, Cheng Y, Kapoor S, Reilly D, Price TS, Fitzgerald GA. Circadian variation of blood pressure and the vascular response to asynchronous stress. Proc Natl Acad Sci U S A. 2007; 104:3450–5.

29. 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. Disruption of the circadian clock within the cardiomyocyte influences myocardial contractile function, metabolism, and gene expression. Am J Physiol Heart Circ Physiol. 2008; 294:H1036–47.

30. Zuber AM, Centeno G, Pradervand S, Nikolaeva S, Maquelin L, Cardinaux L, Bonny O, Firsov D. Molecular clock is involved in predictive circadian adjustment of renal function. Proc Natl Acad Sci U S A. 2009; 106:16523–8.

31. Gumz ML, Stow LR, Lynch IJ, Greenlee MM, Rudin A, Cain BD, Weaver DR, Wingo CS. The circadian clock protein Period 1 regulates expression of the renal epithelial sodium channel in mice. J Clin Invest. 2009; 119:2423–34.

32. Ohkura N, Oishi K, Fukushima N, Kasamatsu M, Atsumi GI, Ishida N, Horie S, Matsuda J. Circadian clock molecules CLOCK and CRYs modulate fibrinolytic activity by regulating the PAI-1 gene expression. J Thromb Haemost. 2006; 4:2478–85.

33. Viswambharan H, Carvas JM, Antic V, Marecic A, Jud C, Zaugg CE, Ming XF, Montani JP, Albrecht U, Yang Z. Mutation of the circadian clock gene Per2 alters vascular endothelial function. Circulation. 2007; 115:2188–95.

34. Woon PY, Kaisaki PJ, Bragança J, Bihoreau MT, Levy JC, Farrall M, Gauguier D. Aryl hydrocarbon receptor nuclear translocator-like (BMAL1) is associated with susceptibility to hypertension and type 2 diabetes. Proc Natl Acad Sci U S A. 2007; 104:14412–7.

35. Knutsson A, Akerstedt T, Jonsson BG, Orth-Gomer K. Increased risk of ischaemic heart disease in shift workers. Lancet. 1986; 2:89–92.

36. Kawachi I, Colditz GA, Stampfer MJ, Willett WC, Manson JE, Speizer FE, Hennekens CH. Prospective study of shift work and risk of coronary heart disease in women. Circulation. 1995; 92:3178–82.

37. Scheer FA, Hilton MF, Mantzoros CS, Shea SA. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc Natl Acad Sci U S A. 2009; 106:4453–8.

38. Sheikh-Ali M, Maharaj J. Circadian clock desynchronisation and metabolic syndrome. Postgrad Med J. 2014; 90:461–6.