“Omics” Approaches for Sleep and Circadian Rhythm Research: Biomarkers for Identifying Differential Vulnerability to Sleep Loss

Current Sleep Medicine Reports

Volumn 1, Issue 1, 2015, Pages 38-46

  Goel, Namni ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Biomarkers; Circadian rhythms; Epigenomics; Individual differences; Metabolomics; Performance; Sleep deprivation; Transcriptomics

Indexed keywords

BIOLOGICAL MARKER;

CHOLESTEROL SYNTHESIS; CIRCADIAN RHYTHM; DNA POLYMORPHISM; DOWN REGULATION; EPIGENETICS; FATIGUE; GENE SEQUENCE; HUMAN; METABOLOMICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SLEEP DEPRIVATION; SLEEP WAKING CYCLE; TRANSCRIPTOMICS; UPREGULATION;

EID: 84944049525     PISSN: None     EISSN: 21986401     Source Type: Journal    
DOI: 10.1007/s40675-014-0003-7     Document Type: Review

References (77)

1. Van Dongen HPA, Dinges DF. Investigating the interaction between the homeostatic and circadian processes of sleep-wake regulation for the prediction of waking neurobehavioral performance. J Sleep Res. 2003;12:181–7.
2. Goel N, Basner M, Rao H, Dinges DF. Circadian rhythms, sleep deprivation and human performance. Prog Mol Biol Transl Sci. 2013;119:155–90.
3. Achermann P, Dijk DJ, Brunner DP, Borbély AA. A model of human sleep homeostasis based on EEG slow-wave activity; quantitative comparison of data and simulations. Brain Res Bull. 1993;31:97–113.
4. Borbély AA. A two process model of sleep regulation. Hum Neurobiol. 1982;1:195–204.
5. Mallis MM, Mejdal S, Nguyen TT, Dinges DF. Summary of the key features of seven biomathematical models of human fatigue and performance. Aviat Space Environ Med. 2004;75:A4–14.
6. Daan S, Beersma DGM, Borbély AA. Timing of human sleep: recovery process gated by a circadian pacemaker. Am J Physiol. 1984;246:R161–78.
7. Achermann P, Borbély AA. Simulation of daytime vigilance by the additive interaction of a homeostatic and a circadian process. Biol Cybern. 1994;71:115–21.
8. Khalsa SBS, Jewett ME, Duffy JF, Czeisler CA. The timing of the human circadian clock is accurately represented by the core body temperature rhythm following phase shifts to a three-cycle light stimulus near the critical zone. J Biol Rhythm. 2000;15:524–30.
9. Edgar DM, Dement WC, Fuller CA. Effect of SCN lesions on sleep in squirrel monkeys: evidence for opponent processes in sleep-wake regulation. J Neurosci. 1993;13:1065–79.
10. Doran SM, Van Dongen HPA, Dinges DF. Sustained attention performance during sleep deprivation: evidence of state instability. Arch Ital Biol. 2001;139:253–67.
11. Banks S, Dinges DF. Behavioral and physiological consequences of sleep restriction in humans. J Clin Sleep Med. 2007;3:519–28.
12. Goel N, Rao H, Durmer JS, Dinges DF. Neurocognitive consequences of sleep deprivation. Semin Neurol. 2009;29:320–39.
13. Lim J, Dinges DF. A meta-analysis of the impact of short-term sleep deprivation on cognitive variables. Psychol Bull. 2010;136:375–89.
14. Van Dongen HPA, Baynard MD, Maislin G, Dinges DF. Systematic interindividual differences in neurobehavioral impairment from sleep loss: evidence of trait-like differential vulnerability. Sleep. 2004;27:423–33.
15. Van Dongen HPA, Maislin G, Dinges DF. Dealing with inter-individual differences in the temporal dynamics of fatigue and performance: importance and techniques. Aviat Space Environ Med. 2004;75:A147–54.
16. Van Dongen HPA, Maislin G, Mullington JM, Dinges DF. The cumulative cost of additional wakefulness: dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation. Sleep. 2003;26:117–26.
17. Goel N, Banks S, Mignot E, Dinges DF. PER3 polymorphism predicts cumulative sleep homeostatic but not neurobehavioral changes to chronic partial sleep deprivation. PLoS One. 2009;4:e5874.
18. Goel N, Banks S, Mignot E, Dinges DF. DQB1*0602 predicts interindividual differences in physiologic sleep, sleepiness and fatigue. Neurology. 2010;75:1509–19.
19. Goel N, Banks S, Lin L, Mignot E, Dinges DF. Catechol-O-methyltransferase Val158Met polymorphism associates with individual differences in sleep physiologic responses to chronic sleep loss. PLoS One. 2011;6:e29283.
20. Bliese PD, Wesensten NJ, Balkin TJ. Age and individual variability in performance during sleep restriction. J Sleep Res. 2006;15:376–85.
21. Van Dongen HPA, Dijkman MV, Maislin G, Dinges DF. Phenotypic aspect of vigilance decrement during sleep deprivation. Physiologist. 1999;42:A-5.
22. Goel N. Genetics of sleep timing, duration and homeostasis in humans. Sleep Med Clin. 2011;6:171–82.
23. Goel N, Dinges DF. Predicting risk in space: genetic markers for differential vulnerability to sleep restriction. Acta Astronaut. 2012;77:207–13.
24. Rao P, Benito E, Fischer A. MicroRNAs as biomarkers for CNS disease. Front Mol Neurosci. 2013;6:39.
25. Mackiewicz M, Zimmerman JE, Shockley KR, Churchill GA, Pack AI. What are microarrays teaching us about sleep? Trends Mol Med. 2009;15:79–87.
26. Cirelli C, Gutierrez CM, Tononi G. Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron. 2004;41:35–43.
27. Terao A, Wisor JP, Peyron C, Apte-Deshpande A, Wurts SW, Edgar DM, et al. Gene expression in the rat brain during sleep deprivation and recovery sleep: an Affymetrix GeneChip study. Neuroscience. 2006;137:593–605.
28. Maret S, Dorsaz S, Gurcel L, Pradervand S, Petit B, Pfister C, et al. Homer1a is a core brain molecular correlate of sleep loss. Proc Natl Acad Sci U S A. 2007;104:20090–5.
29. Mackiewicz M, Shockley KR, Romer MA, Galante RJ, Zimmerman JE, Naidoo N, et al. Macromolecule biosynthesis: a key function of sleep. Physiol Genomics. 2007;31:441–57.
30. Cirelli C, LaVaute TM, Tononi G. Sleep and wakefulness modulate gene expression in Drosophila. J Neurochem. 2005;94:1411–9.
31. Zimmerman JE, Rizzo W, Shockley KR, Raizen DM, Naidoo N, Mackiewicz M, et al. Multiple mechanisms limit the duration of wakefulness in Drosophila brain. Physiol Genomics. 2006;27:337–50.
32. Jones S, Pfister-Genskow M, Benca RM, Cirelli C. Molecular correlates of sleep and wakefulness in the brain of the white-crowned sparrow. J Neurochem. 2008;105:46–62.
33. Wang H, Liu Y, Briesemann M, Yan J. Computational analysis of gene regulation in animal sleep deprivation. Physiol Genomics. 2010;42:427–36.
34. Anafi RC, Pellegrino R, Shockley KR, Romer M, Tufik S, Pack AI. Sleep is not just for the brain: transcriptional responses to sleep in peripheral tissues. BMC Genomics. 2013;14:362.
35. Ackermann K, Plomp R, Lao O, Middleton B, Revell VL, Skene DJ, et al. Effect of sleep deprivation on rhythms of clock gene expression and melatonin in humans. Chronobiol Int. 2013;30:901–9.
36. Möller-Levet CS, Archer SN, Bucca G, Laing EE, Slak A, Kabiljo R, 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:E1132–41. This study demonstrates that one week of sleep restriction alters gene expression, reduces the amplitude of circadian rhythms in gene expression, and intensifies the effects of subsequent acute total sleep loss on gene expression. The affected genes are involved in chromatin remodeling, gene expression regulation and immune and stress responses. The study highlights the molecular interrelationships between sleep homeostasis and circadian rhythmicity.
37. Archer SN, Laing EE, Möller-Levet CS, van der Veen DR, Bucca G, Lazar AS, et al. Mistimed sleep disrupts circadian regulation of the human transcriptome. Proc Natl Acad Sci U S A. 2014;111:E682–91.
38. Pellegrino R, Sunaga DY, Guindalini C, Martins RC, Mazzotti DR, Wei Z, et al. Whole blood genome-wide gene expression profile in males after prolonged wakefulness and sleep recovery. Physiol Genomics. 2012;44:1003–12.
39. Arnardottir ES, Nikonova EV, Shockley KR, Podtelezhnikov AA, Anafi RC, Tanis KQ, et al. Blood-gene expression reveals reduced circadian rhythmicity in individuals resistant to sleep deprivation. Sleep. 2014;37:1589–600. This paper examines whether gene expression changes in blood cells induced by sleep loss are different in individuals resistant and sensitive to acute sleep deprivation. It reports reduced circadian rhythmicity in individuals who are resistant to sleep deprivation, as determined by the Psychomotor Vigilance Test.
40. Lim J, Dinges DF. Sleep deprivation and vigilant attention. Ann N Y Acad Sci. 2008;1129:305–22.
41. Warby SC, Mongrain V. Resisting sleep deprivation by breaking the link between sleep and circadian rhythms. Sleep. 2014;37:1581–2.
42. Stankiewicz AM, Swiergiel AH, Lisowski P. Epigenetics of stress adaptations in the brain. Brain Res Bull. 2013;98:76–92.
43. Nilsen TW. Mechanisms of microRNA-mediated gene regulation in animal cells. Trends Genet. 2007;23:243–9.
44. Chen R, D’Alessandro M, Lee C. miRNAs are required for generating a time delay critical for the circadian oscillator. Curr Biol. 2013;23:1959–68.
45. Davis CJ, Bohnet SG, Meyerson JM, Krueger JM. Sleep loss changes microRNA levels in the brain: a possible mechanism for state-dependent translational regulation. Neurosci Lett. 2007;422:68–73.
46. Davis CJ, Clinton JM, Taishi P, Bohnet SG, Honn KA, Krueger JM. MicroRNA 132 alters sleep and varies with time in brain. J Appl Physiol. 2011;111:665–72.
47. Davis CJ, Clinton JM, Krueger JM. MicroRNA 138, let-7b, and 125a inhibitors differentially alter sleep and EEG delta-wave activity in rats. J Appl Physiol. 2012;113:1756–62.
48. Mongrain V, Hernandez SA, Pradervand S, Dorsaz S, Curie T, Hagiwara G, et al. Separating the contribution of glucocorticoids and wakefulness to the molecular and electrophysiological correlates of sleep homeostasis. Sleep. 2010;33:1147–57.
49. Gharib SA, Khalyfa A, Abdelkarim A, Bhushan B, Gozal D. Integrative miRNA-mRNA profiling of adipose tissue unravels transcriptional circuits induced by sleep fragmentation. PLoS One. 2012;7:e37669.
50. Holm A, Bang-Berthelsen CH, Knudsen S, Kornum BR, Modvig S, Jennum P, et al. miRNA profiles in plasma from patients with sleep disorders reveal dysregulation of miRNAs in narcolepsy and other central hypersomnias. Sleep. 2014;37:1525–33. This study is the first to investigate the role of miRNAs in sleep disorders. It found that 4 miRNAs differed in patients with narcolepsy and other central hypersomnias compared with controls, suggesting that miRNA alterations may be involved in the pathophysiology of these sleep disorders.
51. Cheng HY, Papp JW, Varlamova O, Dziema H, Russell B, Curfman JP, et al. microRNA modulation of circadian-clock period and entrainment. Neuron. 2007;54:813–29.
52. Luo W, Sehgal A. Regulation of circadian behavioral output via a MicroRNA-JAK/STAT circuit. Cell. 2012;148:765–79.
53. Yang M, Lee JE, Padgett RW, Edery I. Circadian regulation of a limited set of conserved microRNAs in Drosophila. BMC Genomics. 2008;9:83.
54. Gatfield D, Le Martelot G, Vejnar CE, Gerlach D, Schaad O, Fleury-Olela F, et al. Integration of microRNA miR-122 in hepatic circadian gene expression. Genes Dev. 2009;23:1313–26.
55. Kadener S, Menet JS, Sugino K, Horwich MD, Weissbein U, Nawathean P, et al. A role for microRNAs in the Drosophila circadian clock. Genes Dev. 2009;23:2179–91.
56. Nagel R, Clijsters L, Agami R. The miRNA-192/194 cluster regulates the period gene family and the circadian clock. FEBS J. 2009;276:5447–55.
57. Du NH, Arpat AB, De Matos M, Gatfield D. MicroRNAs shape circadian hepatic gene expression on a transcriptome-wide scale. eLife. 2014;3:e02510.
58. Shi F, Chen X, Fu A, Hansen J, Stevens R, Tjonneland A, et al. Aberrant DNA methylation of miR-219 promoter in long-term night shiftworkers. Environ Mol Mutagen. 2013;54:406–13.
59. Saus E, Soria V, Escaramís G, Vivarelli F, Crespo JM, Kagerbauer B, et al. Genetic variants and abnormal processing of pre-miR-182, a circadian clock modulator, in major depression patients with late insomnia. Hum Mol Genet. 2010;19:4017–25.
60. Fan HM, Sun XY, Guo W, Zhong AF, Niu W, Zhao L, et al. Differential expression of microRNA in peripheral blood mononuclear cells as specific biomarker for major depressive disorder patients. J Psychiatr Res. 2014;59:45–52.
61. Xu Y, Liu H, Li F, Sun N, Ren Y, Liu Z, et al. A polymorphism in the microRNA-30e precursor associated with major depressive disorder risk and P300 waveform. J Affect Disord. 2010;127:332–6.
62. Rong H, Liu TB, Yang KJ, Yang HC, Wu DH, Liao CP, et al. MicroRNA-134 plasma levels before and after treatment for bipolar mania. J Psychiatr Res. 2011;45:92–5.
63. Mendlewicz J. Disruption of the circadian timing systems: molecular mechanisms in mood disorders. CNS Drugs. 2009;23:15–26.
64. Davies SK, Ang JE, Revell VL, Holmes B, Mann A, Robertson FP, et al. Effect of sleep deprivation on the human metabolome. Proc Natl Acad Sci U S A. 2014;111:10761–6. This paper assesses metabolic profiles during sleep and acute total sleep deprivation and the characterization of 24-hour rhythms under these conditions in healthy males.
65. Eckel-Mahan KL, Patel VR, Mohney RP, Vignola KS, Baldi P, Sassone-Corsi P. Coordination of the transcriptome and metabolome by the circadian clock. Proc Natl Acad Sci U S A. 2012;109:5541–6.
66. Fustin JM, Doi M, Yamada H, Komatsu R, Shimba S, Okamura H. Rhythmic nucleotide synthesis in the liver: temporal segregation of metabolites. Cell Rep. 2012;1:341–9.
67. Minami Y, Kasukawa T, Kakazu Y, Iigo M, Sugimoto M, Ikeda S, et al. Measurement of internal body time by blood metabolomics. Proc Natl Acad Sci U S A. 2009;106:9890–5.
68. Slupsky CM, Rankin KN, Wagner J, Fu H, Chang D, Weljie AM, et al. Investigations of the effects of gender, diurnal variation, and age in human urinary metabolomic profiles. Anal Chem. 2007;79:6995–7004.
69. Walsh MC, Brennan L, Malthouse JP, Roche HM, Gibney MJ. Effect of acute dietary standardization on the urinary, plasma, and salivary metabolomic profiles of healthy humans. Am J Clin Nutr. 2006;84:531–9.
70. Kasukawa T, Sugimoto M, Hida A, Minami Y, Mori M, Honma S, et al. Human blood metabolite timetable indicates internal body time. Proc Natl Acad Sci U S A. 2012;109:15036–41.
71. Dallmann R, Viola AU, Tarokh L, Cajochen C, Brown SA. The human circadian metabolome. Proc Natl Acad Sci U S A. 2012;109:2625–9.
72. Ang JE, Revell V, Mann A, Mäntele S, Otway DT, Johnston JD, et al. Identification of human plasma metabolites exhibiting time-of-day variation using an untargeted liquid chromatography-mass spectrometry metabolomic approach. Chronobiol Int. 2012;29:868–81.
73. Chua EC, Shui G, Lee IT, Lau P, Tan LC, Yeo SC, et al. Extensive diversity in circadian regulation of plasma lipids and evidence for different circadian metabolic phenotypes in humans. Proc Natl Acad Sci U S A. 2013;110:14468–73. This paper used targeted lipidomics-based approaches to profile the time course of 263 lipids in blood plasma in healthy men. The authors report substantial variation in the timing and strength of lipid rhythms across different lipid species, indicating the presence of different circadian metabolic phenotypes in the general population.
74. Bell LN, Kilkus JM, Booth 3rd JN, Bromley LE, Imperial JG, Penev PD. Effects of sleep restriction on the human plasma metabolome. Physiol Behav. 2013;22:25–31.
75. Spaeth AM, Dinges DF, Goel N. Effects of sleep restriction on weight gain, caloric intake and meal timing in healthy adults. Sleep. 2013;36:981–90.
76. Spaeth AM, Dinges DF, Goel N. Sex and race differences in caloric intake during sleep restriction in healthy adults. Am J Clin Nutr. 2014;100:559–66.
77. Schmidt MA, Goodwin TJ. Personalized medicine in human space flight: using Omics based analyses to develop individualized countermeasures that enhance astronaut safety and performance. Metabolomics. 2013;9:1134–56.