The islet circadian clock: Entrainment mechanisms, function and role in glucose homeostasis

Diabetes, Obesity and Metabolism

Volumn 17, Issue S1, 2015, Pages 115-122

  Rakshit, K ^a   Qian, J ^b   Colwell, C S ^b   Matveyenko, A V ^a  

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Circadian clock; Circadian disruption; Insulin secretion; Islet; T2DM; cell

Indexed keywords

BIOLOGICAL MARKER; GLUCOSE; INSULIN;

CELL SURVIVAL; CIRCADIAN RHYTHM; DISEASE ASSOCIATION; ENVIRONMENTAL FACTOR; EXOCYTOSIS; GENE DISRUPTION; GLUCOSE HOMEOSTASIS; HUMAN; INSULIN RELEASE; LIGHT DARK CYCLE; METABOLIC REGULATION; NEUROMODULATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OSCILLATORY POTENTIAL; OXIDATIVE STRESS; PANCREAS ISLET CELL; PANCREAS ISLET CELL FUNCTION; PHENOTYPE; REVIEW; RISK FACTOR; SLEEP WAKING CYCLE; COMPLICATION; DIABETES MELLITUS, TYPE 2; FEEDING BEHAVIOR; HOMEOSTASIS; METABOLIC SYNDROME X; METABOLISM; MITOCHONDRION; PANCREAS ISLET BETA CELL; PHYSIOLOGY; SECRETION (PROCESS); SLEEP DISORDER;

CHRONOBIOLOGY DISORDERS; CIRCADIAN CLOCKS; DIABETES MELLITUS, TYPE 2; EXOCYTOSIS; FEEDING BEHAVIOR; GLUCOSE; HOMEOSTASIS; HUMANS; INSULIN; INSULIN-SECRETING CELLS; METABOLIC SYNDROME X; MITOCHONDRIA; OXIDATIVE STRESS;

EID: 84940571378     PISSN: 14628902     EISSN: 14631326     Source Type: Journal    
DOI: 10.1111/dom.12523     Document Type: Review

References (73)

1. Whiting DR, Guariguata L, Weil C et al. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract 2011; 94: 311-321.
2. Rizza RA. Pathogenesis of fasting and postprandial hyperglycaemia in type 2 diabetes: implications for therapy. Diabetes 2010; 59: 2697-2707.
3. DeFronzo RA, Abdul-Ghani MA. Preservation of beta-cell function: the key to diabetes prevention. J Clin Endocrinol Metab 2011; 96: 2354-2366.
4. Pimenta W, Korytkowski M, Mitrakou A et al. Pancreatic beta-cell dysfunction as the primary genetic lesion in NIDDM. Evidence from studies in normal glucose-tolerant individuals with a first-degree NIDDM relative. JAMA 1995; 273: 1855-1861.
5. Brunzell JD, Robertson RP, Lerner RL et al. Relationships between fasting plasma glucose levels and insulin secretion during intravenous glucose tolerance tests. J Clin Endocrinol Metab 1976; 42: 222-229.
6. Butler AE, Janson J, Bonner-Weir S et al. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 2003; 52: 102-110.
7. Basu A, Dalla Man C, Basu R et al. Effects of type 2 diabetes on insulin secretion, insulin action, glucose effectiveness, and postprandial glucose metabolism. Diabetes Care 2009; 32: 866-872.
8. Porksen N, Hollingdal M, Juhl C et al. Pulsatile insulin secretion: detection, regulation, and role in diabetes. Diabetes 2002; 51(Suppl 1): S245-S254.
9. Hojberg PV, Vilsboll T, Rabol R et al. Four weeks of near-normalisation of blood glucose improves the insulin response to glucagon-like peptide-1 and glucose-dependent insulinotropic polypeptide in patients with type 2 diabetes. Diabetologia 2009; 52: 199-207.
10. Talchai C, Xuan S, Lin HV et al. Pancreatic beta cell dedifferentiation as a mechanism of diabetic beta cell failure. Cell 2012; 150: 1223-1234.
11. Smushkin G, Vella A. Genetics of type 2 diabetes. Curr Opin Clin Nutr Metab Care 2010; 13: 471-477.
12. Yki-Jarvinen H. Role of insulin resistance in the pathogenesis of NIDDM. Diabetologia 1995; 38: 1378-1388.
13. Lin YC, Hsiao TJ, Chen PC. Persistent rotating shift-work exposure accelerates development of metabolic syndrome among middle-aged female employees: a five-year follow-up. Chronobiol Int 2009; 26: 740-755.
14. Pan A, Schernhammer ES, Sun Q et al. Rotating night shift work and risk of type 2 diabetes: two prospective cohort studies in women. PLoS Med 2011; 8: e1001141.
15. Suwazono Y, Dochi M, Oishi M et al. Shiftwork and impaired glucose metabolism: a 14-year cohort study on 7104 male workers. Chronobiol Int 2009; 26: 926-941.
16. Knutson KL, Ryden AM, Mander BA et al. Role of sleep duration and quality in the risk and severity of type 2 diabetes mellitus. Arch Intern Med 2006; 166: 1768-1774.
17. Meisinger C, Heier M, Loewel H. Sleep disturbance as a predictor of type 2 diabetes mellitus in men and women from the general population. Diabetologia 2005; 48: 235-241.
18. Yaggi HK, Araujo AB, McKinlay JB. Sleep duration as a risk factor for the development of type 2 diabetes. Diabetes Care 2006; 29: 657-661.
19. 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: 129ra43.
20. Leproult R, Holmback U, Van Cauter E. Circadian misalignment augments markers of insulin resistance and inflammation, independently of sleep loss. Diabetes 2014; 63: 1860-1869.
21. Qin LQ, Li J, Wang Y et al. The effects of nocturnal life on endocrine circadian patterns in healthy adults. Life Sci 2003; 73: 2467-2475.
22. Scheer FA, Hilton MF, Mantzoros CS et al. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc Natl Acad Sci U S A 2009; 106: 4453-4458.
23. Spiegel K, Leproult R, Van Cauter E. Impact of sleep debt on metabolic and endocrine function. Lancet 1999; 354: 1435-1439.
24. Spiegel K, Tasali E, Leproult R et al. Effects of poor and short sleep on glucose metabolism and obesity risk. Nat Rev Endocrinol 2009; 5: 253-261.
25. Bach AG, Muhlbauer E, Peschke E. Adrenoceptor expression and diurnal rhythms of melatonin and its precursors in the pineal gland of type 2 diabetic Goto-Kakizaki rats. Endocrinology 2010; 151: 2483-2493.
26. Reutrakul S, Hood MM, Crowley SJ et al. Chronotype is independently associated with glycemic control in type 2 diabetes. Diabetes Care 2013; 36: 2523-2529.
27. Takahashi JS, Hong HK, Ko CH et al. The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat Rev Genet 2008; 9: 764-775.
28. Bass J, Takahashi JS. Circadian integration of metabolism and energetics. Science 2010; 330: 1349-1354.
29. Carroll KF, Nestel PJ. Diurnal variation in glucose tolerance and in insulin secretion in man. Diabetes 1973; 22: 333-348.
30. Lee A, Ader M, Bray GA et al. Diurnal variation in glucose tolerance. Cyclic suppression of insulin action and insulin secretion in normal-weight, but not obese, subjects. Diabetes 1992; 41: 750-759.
31. Saad A, Dalla Man C, Nandy DK et al. Diurnal pattern to insulin secretion and insulin action in healthy individuals. Diabetes 2012; 61: 2691-2700.
32. Boden G, Ruiz J, Urbain JL et al. Evidence for a circadian rhythm of insulin secretion. Am J Physiol 1996; 271: E246-E252.
33. Boden G, Chen X, Urbain JL. Evidence for a circadian rhythm of insulin sensitivity in patients with NIDDM caused by cyclic changes in hepatic glucose production. Diabetes 1996; 45: 1044-1050.
34. Boden G, Chen X, Polansky M. Disruption of circadian insulin secretion is associated with reduced glucose uptake in first-degree relatives of patients with type 2 diabetes. Diabetes 1999; 48: 2182-2188.
35. Peschke E, Peschke D. Evidence for a circadian rhythm of insulin release from perifused rat pancreatic islets. Diabetologia 1998; 41: 1085-1092.
36. Delattre E, Cipolla-Neto J, Boschero AC. Diurnal variations in insulin secretion and K+ permeability in isolated rat islets. Clin Exp Pharmacol Physiol 1999; 26: 505-510.
37. Kalsbeek A, Strubbe JH. Circadian control of insulin secretion is independent of the temporal distribution of feeding. Physiol Behav 1998; 63: 553-558.
38. la Fleur SE, Kalsbeek A, Wortel J et al. A daily rhythm in glucose tolerance: a role for the suprachiasmatic nucleus. Diabetes 2001; 50: 1237-1243.
39. Qian J, Block GD, Colwell CS et al. Consequences of exposure to light at night on the pancreatic islet circadian clock and function in rats. Diabetes 2013; 62: 3469-3478.
40. Reppert SM, Weaver DR. Coordination of circadian timing in mammals. Nature 2002; 418: 935-941.
41. Yoo SH, Yamazaki S, Lowrey PL et al. PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci U S A 2004; 101: 5339-5346.
42. Marcheva B, Ramsey KM, Buhr ED et al. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 2010; 466: 627-631.
43. Pulimeno P, Mannic T, Sage D et al. Autonomous and self-sustained circadian oscillators displayed in human islet cells. Diabetologia 2013; 56: 497-507.
44. Buijs RM, Kalsbeek A. Hypothalamic integration of central and peripheral clocks. Nat Rev Neurosci 2001; 2: 521-526.
45. Gekakis N, Staknis D, Nguyen HB et al. Role of the CLOCK protein in the mammalian circadian mechanism. Science 1998; 280: 1564-1569.
46. Lee C, Etchegaray JP, Cagampang FR et al. Posttranslational mechanisms regulate the mammalian circadian clock. Cell 2001; 107: 855-867.
47. Rakshit K, Thomas AP, Matveyenko AV. Does disruption of circadian rhythms contribute to beta-cell failure in type 2 diabetes? Curr Diab Rep 2014; 14: 474.
48. Asher G, Schibler U. Crosstalk between components of circadian and metabolic cycles in mammals. Cell Metab 2011; 13: 125-137.
49. Kalsbeek A, Palm IF, La Fleur SE et al. SCN outputs and the hypothalamic balance of life. J Biol Rhythms 2006; 21: 458-469.
50. Okamura H. Suprachiasmatic nucleus clock time in the mammalian circadian system. Cold Spring Harb Symp Quant Biol 2007; 72: 551-556.
51. Saini C, Suter DM, Liani A et al. The mammalian circadian timing system: synchronization of peripheral clocks. Cold Spring Harb Symp Quant Biol 2011; 76: 39-47.
52. 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; 14: 2950-2961.
53. Stokkan KA, Yamazaki S, Tei H et al. Entrainment of the circadian clock in the liver by feeding. Science 2001; 291: 490-493.
54. Hirota T, Okano T, Kokame K et al. Glucose down-regulates Per1 and Per2 mRNA levels and induces circadian gene expression in cultured Rat-1 fibroblasts. J Biol Chem 2002; 277: 44244-44251.
55. Rutter J, Reick M, McKnight SL. Metabolism and the control of circadian rhythms. Annu Rev Biochem 2002; 71: 307-331.
56. Jordan SD, Lamia KA. AMPK at the crossroads of circadian clocks and metabolism. Mol Cell Endocrinol 2013; 366: 163-169.
57. Gil-Lozano M, Mingomataj EL, Wu WK et al. Circadian secretion of the intestinal hormone GLP-1 by the rodent L cell. Diabetes 2014; 63: 3674-3685.
58. O'Neill JS, Maywood ES, Chesham JE et al. cAMP-dependent signaling as a core component of the mammalian circadian pacemaker. Science 2008; 320: 949-953.
59. Chaves I, van der Horst GT, Schellevis R et al. Insulin-FOXO3 signaling modulates circadian rhythms via regulation of clock transcription. Curr Biol 2014; 24: 1248-1255.
60. Buhr ED, Yoo SH, Takahashi JS. Temperature as a universal resetting cue for mammalian circadian oscillators. Science 2010; 330: 379-385.
61. Reddy AB, O'Neill JS. Healthy clocks, healthy body, healthy mind. Trends Cell Biol 2010; 20: 36-44.
62. Silva CM, Sato S, Margolis RN. No time to lose: workshop on circadian rhythms and metabolic disease. Genes Dev 2010; 24: 1456-1464.
63. Gale JE, Cox HI, Qian J et al. Disruption of circadian rhythms accelerates development of diabetes through pancreatic beta-cell loss and dysfunction. J Biol Rhythms 2011; 26: 423-433.
64. Matveyenko AV, Gurlo T, Daval M et al. Successful versus failed adaptation to high-fat diet-induced insulin resistance: the role of IAPP-induced beta-cell endoplasmic reticulum stress. Diabetes 2009; 58: 906-916.
65. Lee J, Moulik M, Fang Z et al. Bmal1 and beta-cell clock are required for adaptation to circadian disruption, and their loss of function leads to oxidative stress-induced beta-cell failure in mice. Mol Cell Biol 2013; 33: 2327-2338.
66. Ma X, Idle JR, Krausz KW et al. Metabolism of melatonin by human cytochromes p450. Drug Metab Dispos 2005; 33: 489-494.
67. Sadacca LA, Lamia KA, de Lemos AS et al. An intrinsic circadian clock of the pancreas is required for normal insulin release and glucose homeostasis in mice. Diabetologia 2011; 54: 120-124.
68. Maechler P, Wollheim CB. Mitochondrial function in normal and diabetic beta-cells. Nature 2001; 414: 807-812.
69. Peek CB, Affinati AH, Ramsey KM et al. Circadian clock NAD+ cycle drives mitochondrial oxidative metabolism in mice. Science 2013; 342: 1243417.
70. Rivera JF, Costes S, Gurlo T et al. Autophagy defends pancreatic beta cells from human islet amyloid polypeptide-induced toxicity. J Clin Invest 2014; 124: 3489-3500.
71. Robertson RP, Harmon J, Tran PO et al. Beta-cell glucose toxicity, lipotoxicity, and chronic oxidative stress in type 2 diabetes. Diabetes 2004; 53(Suppl 1): S119-S124.
72. Costes S, Boss M, Thomas AP et al. Activation of melatonin signaling promotes beta-cell survival and function. Mol Endocrinol 2015; 29: 682-692.
73. Nishiyama K, Hirai K. The melatonin agonist Ramelteon induces duration-dependent clock gene expression through cAMP signaling in pancreatic INS-1 beta-cells. PLoS One 2014; 9: e102073.