Short-term sleep deprivation with nocturnal light exposure alters timedependent glucagon-like peptide-1 and insulin secretion in male volunteers

American Journal of Physiology - Endocrinology and Metabolism

Volumn 310, Issue 1, 2015, Pages E41-E50

  Gil Lozano, Manuel ^a   Hunter, Paola M ^a   Behan, Lucy Ann ^a,b   Gladanac, Bojana ^a,b   Casper, Robert F ^a,b   Brubaker, Patricia L ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

Author keywords

Circadian rhythms; Clock genes; Incretin light; Metabolism; Sleep

Indexed keywords

GLUCAGON LIKE PEPTIDE 1; GLUCOSE; HYDROCORTISONE; INSULIN; MELATONIN; TRANSCRIPTION FACTOR CLOCK;

ADULT; AREA UNDER THE CURVE; ARTICLE; CIRCADIAN RHYTHM; FOOD INTAKE; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IN VITRO STUDY; INSULIN RELEASE; INSULIN RESPONSE; L CELL LINE; LIGHT DARK CYCLE; LIGHT EXPOSURE; MALE; NIGHT SLEEP; NORMAL HUMAN; ORAL GLUCOSE TOLERANCE TEST; PRIORITY JOURNAL; SHIFT WORKER; SLEEP DEPRIVATION; ADOLESCENT; CELL CULTURE; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; GENETICS; LIGHT; METABOLISM; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PHYSIOLOGY; RADIATION RESPONSE; SECRETION (PROCESS); TIME FACTOR; YOUNG ADULT;

ADOLESCENT; ADULT; CELLS, CULTURED; CIRCADIAN RHYTHM; CLOCK PROTEINS; GLUCAGON-LIKE PEPTIDE 1; GLUCAGON-SECRETING CELLS; HEALTHY VOLUNTEERS; HUMANS; INSULIN; INSULIN-SECRETING CELLS; LIGHT; MALE; METABOLIC NETWORKS AND PATHWAYS; SLEEP DEPRIVATION; TIME FACTORS; YOUNG ADULT;

EID: 84949564113     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00298.2015     Document Type: Article

References (47)

1. Ahrén B. Incretin hormones and the up-regulation of insulin secretion in insulin resistance. J Clin Endocrinol Metab 97: 1173–1175, 2012.
2. Akerstedt T. Shift work and disturbed sleep/wakefulness. Occup Med (Lond) 53: 89–94, 2003.
3. Anini Y, Brubaker PL. Muscarinic receptors control glucagon-like peptide 1 secretion by human endocrine L cells. Endocrinology 144: 3244–3250, 2003.
4. Berkus MD, Stern MP, Mitchell BD, Newton ER, Langer O. Does fasting interval affect the glucose challenge test? Am J Obstet Gynecol 163: 1812–1817, 1990.
5. Bolli GB, De Feo P, De Cosmo S, Perriello G, Ventura MM, Calcinaro F, Lolli C, Campbell P, Brunetti P, Gerich JE. Demonstration of a dawn phenomenon in normal human volunteers. Diabetes 33: 1150–1153, 1984.
6. Buxton OM, Pavlova M, Reid EW, Wang W, Simonson DC, Adler GK. Sleep restriction for 1 week reduces insulin sensitivity in healthy men. Diabetes 59: 2126–2133, 2010.
7. Cagnacci A, Arangino S, Renzi A, Paoletti AM, Melis GB, Cagnacci P, Volpe A. Influence of melatonin administration on glucose tolerance and insulin sensitivity of postmenopausal women. Clin Endocrinol (Oxf) 54: 339–346, 2001.
8. Cipolla-Neto J, Amaral FG, Afeche SC, Tan DX, Reiter RJ. Melatonin, energy metabolism, and obesity: a review. J Pineal Res 56: 371–381, 2014.
9. Coomans CP, van den Berg SA, Houben T, van Klinken JB, van den Berg R, Pronk AC, Havekes LM, Romijn JA, van Dijk KW, Biermasz NR, Meijer JH. Detrimental effects of constant light exposure and high-fat diet on circadian energy metabolism and insulin sensitivity. FASEB J 7: 1721–1732, 2013.
10. Coomans CP, van den Berg SA, Lucassen EA, Houben T, Pronk AC, van der Spek RD, Kalsbeek A, Biermasz NR, Willems van Dijk K, Romijn JA, Meijer JH. The suprachiasmatic nucleus controls circadian energy met abolism and hepatic insulin sensitivity. Diabetes 62: 1102–1108, 2013.
11. Costes S, Boss M, Thomas AP, Matveyenko AV. Activation of melatonin signaling promotes -cell survival and function. Mol Endocrinol 29: 682–692, 2015.
12. Donga E, van Dijk M, van Dijk JG, Biermasz NR, Lammers GJ, van Kralingen KW, Corssmit EP, Romijn JA. A single night of partial sleep deprivation induces insulin resistance in multiple metabolic pathways in healthy subjects. J Clin Endocrinol Metab 95: 2963–2968, 2010.
13. Edwards CM, Todd JF, Mahmoudi M, Wang Z, Wang RM, Ghatei MA, Bloom SR. Glucagon-like peptide 1 has a physiological role in the control of postprandial glucose in humans: studies with the antagonist exendin 9–39. Diabetes 48: 86–93, 1999.
14. Elliott RM, Morgan LM, Tredger JA, Deacon S, Wright J, Marks V. Glucagon-like peptide-1 (7–36)amide and glucose-dependent insulinotropic polypeptide secretion in response to nutrient ingestion in man: acute post-prandial and 24-h secretion patterns. J Endocrinol 138: 159–166, 1993.
15. Faerch K, Borch-Johnsen K, Vaag A, Jørgensen T, Witte DR. Sex differences in glucose levels: a consequence of physiology or methodological convenience? The Inter99 study. Diabetologia 53: 858–865, 2010.
16. Froy O. Metabolism and circadian rhythms—implications for obesity. Endocr Rev 31: 1–24, 2010.
17. Gibbs M, Harrington D, Starkey S, Williams P, Hampton S. Diurnal postprandial responses to low and high glycaemic index mixed meals. Clin Nutr 33: 889–894, 2014.
18. Gil-Lozano M, Mingomataj EL, Wu WK, Ridout SA, Brubaker PL. Circadian secretion of the intestinal hormone, glucagon-like peptide-1, by the rodent L-cell. Diabetes 63: 3674–3685, 2014.
19. González-Ortiz M, Martínez-Abundis E, Balcázar-Muñoz BR, Pascoe-González S. Effect of sleep deprivation on insulin sensitivity and cortisol concentration in healthy subjects. Diabetes Nutr Metab 13: 80–83, 2000.
20. Goo RH, Moore JG, Greenberg E, Alazraki NP. Circadian variation in gastric emptying of meals in humans. Gastroenterology 93: 515–518, 1987.
21. Jarrett RJ, Baker IA, Keen H, Oakley NW. Diurnal variation in oral glucose tolerance: blood sugar and plasma insulin levels morning, afternoon, and evening. Br Med J 1: 199–201, 1972.
22. Kemp DM, Ubeda M, Habener JF. Identification and functional characterization of melatonin Mel 1a receptors in pancreatic beta cells: potential role in incretin-mediated cell function by sensitization of cAMP signaling. Mol Cell Endocrinol 191: 157–166, 2002.
23. Leproult R, Copinschi G, Buxton O, Van Cauter E. Sleep loss results in an elevation of cortisol levels the next evening. Sleep 20: 865–870, 1997.
24. Lindgren O, Mari A, Deacon CF, Carr RD, Winzell MS, Vikman J, Ahrén B. Differential islet and incretin hormone responses in morning versus afternoon after standardized meal in healthy men. J Clin Endocrinol Metab 94: 288728–288792, 2009.
25. Lund HG, Reider BD, Whiting AB, Prichard JR. Sleep patterns and predictors of disturbed sleep in a large population of college students. J Adolesc Health 46: 124–132, 2010.
26. Marathe CS, Rayner CK, Jones KL, Horowitz M. Relationships between gastric emptying, postprandial glycemia, and incretin hormones. Diabetes Care 36: 1396–1405, 2013.
27. 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 466: 627–631, 2010.
28. Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care 22: 1462–1470, 1999.
29. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and betacell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28: 412–419, 1985.
30. McMullan CJ, Curhan GC, Schernhammer ES, Forman JP. Association of nocturnal melatonin secretion with insulin resistance in nondiabetic young women. Am J Epidemiol 178: 231–238, 2013.
31. McMullan CJ, Schernhammer ES, Rimm EB, Hu FB, Forman JP. Melatonin secretion and the incidence of type 2 diabetes. JAMA 309: 1388–1396, 2013.
32. Nedeltcheva AV, Kessler L, Imperial J, Penev PD. Exposure to recurrent sleep restriction in the setting of high caloric intake and physical inactivity results in increased insulin resistance and reduced glucose tolerance. J Clin Endocrinol Metab 94: 3242–3250, 2009.
33. Ohkuma T, Fujii H, Iwase M, Kikuchi Y, Ogata S, Idewaki Y, Ide H, Doi Y, Hirakawa Y, Nakamura U, Kitazono T. Impact of sleep duration on obesity and the glycemic level in patients with type 2 diabetes: the Fukuoka Diabetes Registry. Diabetes Care 36: 611–617, 2013.
34. Qian J, Block GD, Colwell CS, Matveyenko AV. Consequences of exposure to light at night on the pancreatic islet circadian clock and function in rats. Diabetes 62: 3469–3478, 2013.
35. Rahman SA, Marcu S, Shapiro CM, Brown TJ, Casper RF. Spectral modulation attenuates molecular, endocrine, and neurobehavioral disruption induced by nocturnal light exposure. Am J Physiol Endocrinol Metab 300: E518–E527, 2011.
36. Reimer RA, Darimont C, Gremlich S, Nicolas-Métral V, Rüegg UT, Macé K. A human cellular model for studying the regulation of glucagonlike peptide-1 secretion. Endocrinology 142: 4522–4528, 2001.
37. Rubio-Sastre P, Scheer FA, Gómez-Abellán P, Madrid JA, Garaulet M. Acute melatonin administration in humans impairs glucose tolerance in both the morning and evening. Sleep 37: 1715–1719, 2014.
38. Schmid SM, Hallschmid M, Jauch-Chara K, Wilms B, Lehnert H, Born J, Schultes B. Disturbed glucoregulatory response to food intake after moderate sleep restriction. Sleep 34: 371–377, 2011.
39. Selimoglu H, Duran C, Kiyici S, Guclu M, Ersoy C, Ozkaya G, Erturk E, Tuncel E, Imamoglu S. Comparison of composite whole body insulin sensitivity index derived from mixed meal test and oral glucose tolerance test in insulin resistant obese subjects. Endocrine 36: 299–304, 2009.
40. Simpson AK, Ward PS, Wong KY, Collord GJ, Habib AM, Reimann F, Gribble FM. Cyclic AMP triggers glucagon-like peptide-1 secretion from the GLUTag enteroendocrine cell line. Diabetologia 50: 2181–2189, 2007.
41. Spiegel K, Leproult R, Van Cauter E. Impact of sleep debt on metabolic and endocrine function. Lancet 354: 1435–1439, 1999.
42. Suwazono Y, Sakata K, Okubo Y, Harada H, Oishi M, Kobayashi E, Uetani M, Kido T, Nogawa K. Long-term longitudinal study on the relationship between alternating shift work and the onset of diabetes mellitus in male Japanese workers. J Occup Environ Med 48: 455–461, 2006.
43. Van Cauter E, Blackman JD, Roland D, Spire JP, Refetoff S, Polonsky KS. Modulation of glucose regulation and insulin secretion by circadian rhythmicity and sleep. J Clin Invest 88: 934–942, 1991.
44. VanHelder T, Symons JD, Radomski MW. Effects of sleep deprivation and exercise on glucose tolerance. Aviat Space Environ Med 64: 487–492, 1993.
45. Vilsbøll T, Krarup T, Sonne J, Madsbad S, Vølund A, Juul AG, Holst JJ. Incretin secretion in relation to meal size and body weight in healthy subjects and people with type 1 and type 2 diabetes mellitus. J Clin Endocrinol Metab 88: 2706–2713, 2003.
46. Wallace TM, Levy JC, Matthews DR. Use and abuse of HOMA modeling. Diabetes Care 27: 1487–1495, 2004.
47. Zimmet PZ, Wall JR, Rome R, Stimmler L, Jarrett RJ. Diurnal variation in glucose tolerance: associated changes in plasma insulin, growth hormone, and non-esterified fatty acids. Br Med J 1: 485–488, 1974.