Acute sleep loss induces tissue-specific epigenetic and transcriptional alterations to circadian clock genes in men

Journal of Clinical Endocrinology and Metabolism

Volumn 100, Issue 9, 2015, Pages E1255-E1261

  Cedernaes, Jonathan ^a   Osler, Megan E ^b   Voisin, Sarah ^a   Broman, Jan Erik ^a   Vogel, Heike ^c,d   Dickson, Suzanne L ^d   Zierath, Juleen R ^b   Schiöth, Helgi B ^a   Benedict, Christian ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; HYDROCORTISONE; TRANSCRIPTION FACTOR CLOCK; CIRCADIAN RHYTHM SIGNALING PROTEIN; CRY1 PROTEIN, HUMAN; CRYPTOCHROME; GLUCOSE BLOOD LEVEL; PER1 PROTEIN, HUMAN; TRANSCRIPTION FACTOR ARNTL;

ARTICLE; BIOPSY; BMAL1 GENE; CLOCK GENE; CONTROLLED STUDY; CRY1 GENE; DNA METHYLATION; EPIGENETICS; GENE; GENE EXPRESSION; GENE INTERACTION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; GLUCOSE BLOOD LEVEL; HORMONE DETERMINATION; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; HYDROCORTISONE BLOOD LEVEL; MALE; MUSCLE BIOPSY; NORMAL HUMAN; ORAL GLUCOSE TOLERANCE TEST; PER1 GENE; PRIORITY JOURNAL; PROMOTER REGION; RANDOMIZED CONTROLLED TRIAL; SLEEP DEPRIVATION; SUBCUTANEOUS ADIPOSE TISSUE BIOPSY; TISSUE SPECIFICITY; WAKEFULNESS; BLOOD; CIRCADIAN RHYTHM; CROSSOVER PROCEDURE; GENETIC EPIGENESIS; GENETICS; METABOLISM; SKELETAL MUSCLE; SLEEP; YOUNG ADULT;

ARNTL TRANSCRIPTION FACTORS; BLOOD GLUCOSE; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; CLOCK PROTEINS; CROSS-OVER STUDIES; CRYPTOCHROMES; EPIGENESIS, GENETIC; GENE EXPRESSION; HUMANS; HYDROCORTISONE; MALE; MUSCLE, SKELETAL; PERIOD CIRCADIAN PROTEINS; SLEEP; SLEEP DEPRIVATION; YOUNG ADULT;

EID: 84941703109     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/JC.2015-2284     Document Type: Article

References (42)

1. Bass J. Circadian topology of metabolism. Nature. 2012;491:348-356.
2. Dyar KA, Ciciliot S, Wright LE, et al. Muscle insulin sensitivity and glucose metabolism are controlled by the intrinsic muscle clock. Mol Metab. 2014;3:29-41.
3. Paschos GK, Ibrahim S, Song WL, et al. Obesity in mice with adipocyte-specific deletion of clock component Arntl. Nat Med. 2012; 18:1768-1777.
4. 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.
5. Turek FW, Joshu C, Kohsaka A, et al. Obesity and metabolic syndrome in circadian Clock mutant mice. Science. 2005;308:1043-1045.
6. Cedernaes J, Schiöth HB, Benedict C. Determinants of shortened, disrupted, and mistimed sleep and associated metabolic health consequences in healthy humans. Diabetes. 2015;64:1073-1080.
7. Schmid SM, Hallschmid M, Schultes B. The metabolic burden of sleep loss. Lancet Diabetes Endocrinol. 2015;3(1):52- 62.
8. Möller -Levet CS, Archer SN, Bucca G, et al. Effects of insufficient sleep on circadian rhythmicity and expression amplitude of the human blood transcriptome. Proc Natl Acad Sci U S A. 2013;110: E1132-E1141.
9. Kundaje A, Meuleman W, Ernst J, et al. Integrative analysis of 111 reference human epigenomes. Nature. 2015;518:317-330.
10. Barres R, Yan J, Egan B, et al. Acute exercise remodels promoter methylation in human skeletal muscle. Cell Metab. 2012;15:405-411.
11. Teschendorff AE, Marabita F, Lechner M, et al. A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data. Bioinformatics. 2013;29:189-196.
12. Johnson WE, Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics. 2007;8:118-127.
13. Andersson R, Gebhard C, Miguel-Escalada I, et al. An atlas of active enhancers across human cell types and tissues. Nature. 2014;507: 455-461.
14. HillmerAM,Yao F, Inaki K, et al. Comprehensive long-span pairedend-tag mapping reveals characteristic patterns of structural variations in epithelial cancer genomes. Genome Res. 2011;21:665-675.
15. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I. Controlling the false discovery rate in behavior genetics research. Behav Brain Res. 2001;125:279-284.
16. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402-408.
17. Du P, Zhang X, Huang CC, et al. Comparison of Beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics. 2010;11:587.
18. Milagro FI, Gómez-Abellán P, Campión J, Martnez JA, Ordovás JM, Garaulet M. CLOCK, PER2 and BMAL1 DNA methylation: Association with obesity and metabolic syndrome characteristics and monounsaturated fat intake. Chronobiol Int. 2012;29:1180-1194.
19. Zhu Y, Stevens RG, Hoffman AE, et al. Epigenetic impact of longterm shiftwork: Pilot evidence from circadian genes and whole-genome methylation analysis. Chronobiol Int. 2011;28:852-861.
20. Lamia KA, Papp SJ, Yu RT, et al. Cryptochromes mediate rhythmic repression of the glucocorticoid receptor. Nature. 2011;480:552-556.
21. Ando H, Takamura T, Matsuzawa-Nagata N, et al. Clock gene expression in peripheral leucocytes of patients with type 2 diabetes. Diabetologia. 2009;52:329-335.
22. Benedict C, Hallschmid M, Lassen A, et al. Acute sleep deprivation reduces energy expenditure in healthy men. m J Clin Nutr. 2011; 93:1229-1236.
23. Backhaus J, Junghanns K, Hohagen F. Sleep disturbances are correlated with decreased morning awakening salivary cortisol. Psychoneuroendocrinology. 2004;29(9):1184-91.
24. Balsalobre A, Brown SA, Marcacci L, et al. Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science. 2000; 289:2344-2347.
25. Yamazaki S, Numano R, Abe M, et al. Resetting central and peripheral circadian oscillators in transgenic rats. Science. 2000;288: 682-685.
26. Arendt J. Shift work: Coping with the biological clock. Occup Med. 2010;60:10-20.
27. Bass J, Takahashi JS. Circadian integration of metabolism and energetics. Science. 2010;330:1349-1354.
28. Eckel-Mahan K, Sassone-Corsi P. Metabolism and the circadian clock converge. Physiol Rev. 2013;93:107-135.
29. McDearmon EL, Patel KN, Ko CH, et al. Dissecting the functions of the mammalian clock protein BMAL1 by tissue-specific rescue in mice. Science. 2006;314:1304-1308.
30. Broussard JL, Ehrmann DA, Van Cauter E, Tasali E, Brady MJ. Impaired insulin signaling in human adipocytes after experimental sleep restriction: A randomized, crossover study. Ann Intern Med. 2012;157:549-557.
31. Vondra K, Brodan V, Bass A, et al. Effects of sleep deprivation on the activity of selected metabolic enzymes in skeletal muscle. Eur J Appl Physiol Occup Physiol. 1981;47:41-46.
32. Wright KP Jr, McHill AW, Birks BR, Griffin BR, Rusterholz T, Chinoy ED. Entrainment of thehumancircadian clock to the natural light-dark cycle. Curr Biol. 2013;23(16):1554-1558.
33. Liu C, Li S, Liu T, Borjigin J, Lin JD. Transcriptional coactivator PGC-1alpha integrates the mammalian clock and energy metabolism. Nature. 2007;447:477-481.
34. Nagaya T, Yoshida H, Takahashi H, Kawai M. Markers of insulin resistance in day and shift workers aged 30-59 years. Int Arch Occup Environ Health. 2002;75:562-568.
35. 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;4:129ra143.
36. Leproult R, Holmbäck U, Van Cauter E. Circadian misalignment augments markers of insulin resistance and inflammation, independently of sleep loss. Diabetes. 2014;63:1860-1869.
37. Rao MN, Neylan TC, Grunfeld C, Mulligan K, Schambelan M, Schwarz JM. Subchronic sleep restriction causes tissue-specific insulin resistance. J Clin Endocrinol Metab. 2015;100(4):1664-1671.
38. Dopico XC, Evangelou M, Ferreira RC, et al. Widespread seasonal gene expression reveals annual differences in human immunity and physiology. Nat Commun. 2015;6:7000.
39. Chang AM, Aeschbach D, Duffy JF, Czeisler CA. Evening use of light-emitting eReaders negatively affects sleep, circadian timing, and next-morning alertness. Proc Natl Acad SciUSA. 2015;112(4): 1232-1237.
40. Izumo M, Pejchal M, Schook AC, et al. Differential effects of light and feeding on circadian organization of peripheral clocks in a forebrain Bmal1 mutant. Elife. 2014;3.
41. Scheer FA, Buijs RM. Light affects morning salivary cortisol in humans. J Clin Endocrinol Metab. 1999;84:3395-3398.
42. Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M. Entrainment of the circadian clock in the liver by feeding. Science. 2001; 291:490-493.