Epigenetics of sleep and chronobiology

Current Neurology and Neuroscience Reports

Volumn 14, Issue 3, 2014, Pages

  Qureshi, Irfan A ^a   Mehler, Mark F ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Chromatin; Circadian; DNA methylation; Epigenetic; Histonemodification; Long noncoding RNA; MicroRNA; Noncoding RNA; RNA editing; Sleep

Indexed keywords

UNTRANSLATED RNA;

CHROMATIN ASSEMBLY AND DISASSEMBLY; CHRONOBIOLOGY; CIRCADIAN RHYTHM; COMORBIDITY; DNA METHYLATION; DNA MODIFICATION; EPIGENETICS; GENE FUNCTION; GENE MUTATION; HUMAN; NONHUMAN; PATHOGENESIS; PROTEIN MODIFICATION; REVIEW; RNA EDITING; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SLEEP; SLEEP DISORDER; SLEEP WAKING CYCLE; SUPRACHIASMATIC NUCLEUS; TRANSCRIPTION REGULATION; ANIMAL; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; PHYSIOLOGY;

ANIMALS; CIRCADIAN RHYTHM; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HUMANS; SLEEP; SLEEP DISORDERS; SUPRACHIASMATIC NUCLEUS;

EID: 84892946733     PISSN: 15284042     EISSN: 15346293     Source Type: Journal    
DOI: 10.1007/s11910-013-0432-6     Document Type: Review

References (88)

1. Mehler MF. Epigenetic principles and mechanisms underlying nervous system functions in health and disease. Prog Neurobiol. 2008;86:305-41.
2. Qureshi IA, Mehler MF. Emerging roles of noncoding RNAs in brain evolution, development, plasticity and disease. Nat Rev Neurosci. 2012;13:528-41.
3. Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotechnol [Review]. 2010;28:1057-68.
4. Qureshi IA,Mehler MF. Understanding neurological disease-mechanisms in the era of epigenetics. JAMA Neurol. 2013;70:703-10.
5. Qureshi IA, Mehler MF. Developing epigenetic diagnostics and therapeutics for brain disorders. Trends Mol Med. 2013;19(12):732-41.
6. Qureshi IA, Mehler MF. Long noncoding RNAs: novel targets for nervous system disease diagnosis and therapy. Neurotherapeutics. 2013;10:632-46.
7. Masri S, Sassone-Corsi P. The circadian clock: a framework linking metabolism, epigenetics and neuronal function. Nat Rev Neurosci. 2012;14:69-75.
8. Albrecht U. Timing to perfection: the biology of central and peripheral circadian clocks. Neuron. 2012;74:246-60.
9. Lim C, Allada R. Emerging roles for post-transcriptional regulation in circadian clocks. Nat Neurosci. 2013;16:1544-50.
10. Mellen M, Ayata P, Dewell S, et al. MeCP2 Binds to 5hmC enriched within active genes and accessible chromatin in the nervous system. Cell. 2012;151:1417-30.
11. Jin SG, Wu X, Li AX, Pfeifer GP. Genomic mapping of 5- hydroxymethylcytosine in the human brain. Nucleic Acids Res. 2011;39:5015-24.
12. Bonsch D, Hothorn T, Krieglstein C, et al. Daily variations of homocysteine concentration may influence methylation of DNA in normal healthy individuals. Chronobiol Int. 2007;24:315-26.
13. Li JZ, Bunney BG, Meng F, et al. Circadian patterns of gene expression in the human brain and disruption in major depressive disorder. Proc Natl Acad Sci U S A. 2013;110:9950-5.
14. Maekawa F, Shimba S, Takumi S, et al. Diurnal expression of Dnmt3b mRNA in mouse liver is regulated by feeding and hepatic clockwork. Epigenetics. 2012;7:1046-56.
15. Zhou Z, Hong EJ, Cohen S, et al. Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron. 2006;52:255-69. (Pubitemid 44548348)
16. BeldenWJ, Lewis ZA, Selker EU, et al. CHD1 remodels chromatin and influences transient DNA methylation at the clock gene frequency. PLoS Genet. 2011;7:e1002166.
17. Ji Y, Qin Y, Shu H, Li X. Methylation analyses on promoters of mPer1, mPer2, and mCry1 during perinatal development. Biochem Biophys Res Commun. 2010;391:1742-7.
18. Zhang L, Lin QL, Lu L, et al. Tissue-specific modification of clock methylation in aging mice. Eur Rev Med Pharmacol Sci. 2013;17:1874-80.
19. Nakatome M, Orii M, Hamajima M, et al. Methylation analysis of circadian clock gene promoters in forensic autopsy specimens. Leg Med. 2011;13:205-9.
20. Neumann O, Kesselmeier M, Geffers R, et al. Methylome analysis and integrative profiling of human HCCs identify novel protumorigenic factors. Hepatology. 2012;56:1817-27.
21. Hanoun M, Eisele L, Suzuki M, et al. Epigenetic silencing of the circadian clock gene CRY1 is associated with an indolent clinical course in chronic lymphocytic leukemia. PLoS One. 2012;7:e34347.
22. Hoffman AE, Zheng T, Yi CH, et al. The core circadian gene Cryptochrome 2 influences breast cancer risk, possibly by mediating hormone signaling. Cancer Prev Res. 2010;3:539-48.
23. Taniguchi H, Fernandez AF, Setien F, et al. Epigenetic inactivation of the circadian clock gene BMAL1 in hematologic malignancies. Cancer Res. 2009;69:8447-54.
24. Milagro FI, Gomez-Abellan P, Campion J, et al. CLOCK, PER2 and BMAL1 DNA methylation: association with obesity and metabolic syndrome characteristics and monounsaturated fat intake. Chronobiol Int. 2012;29:1180-94.
25. Wither RG, Colic S, Wu C, et al. Daily rhythmic behaviors and thermoregulatory patterns are disrupted in adult female MeCP2-deficient mice. PLoS One. 2012;7:e35396.
26. •• Nanduri J,Makarenko V, Reddy VD, et al. Epigenetic regulation of hypoxic sensing disrupts cardiorespiratory homeostasis. Proc Natl Acad Sci U S A. 2012;109:2515-20. This paper demonstrated that DNA methylation plays a role in the neonatal programming of hypoxic sensitivity and subsequent autonomic deregulation during adulthood.
27. Young D, Nagarajan L, de Klerk N, et al. Sleep problems in Rett syndrome. Brain Dev. 2007;29:609-16. (Pubitemid 47419209)
28. Winkelmann J, Lin L, Schormair B, et al. Mutations in DNMT1 cause autosomal dominant cerebellar ataxia, deafness and narcolepsy. Hum Mol Genet. 2012;21:2205-10.
29. Pedroso JL, Povoas Barsottini OG, Lin L, et al. A novel de novo exon 21 DNMT1 mutation causes cerebellar ataxia, deafness, and narcolepsy in a Brazilian patient. Sleep. 2013;36:1257-9, 59A.
30. Syeda F, Fagan RL, Wean M, et al. The replication focus targeting sequence (RFTS) domain is a DNA-competitive inhibitor of Dnmt1. J Biol Chem. 2011;286:15344-51.
31. Bollati V, Baccarelli A, Sartori S, et al. Epigenetic effects of shiftwork on blood DNA methylation. Chronobiol Int. 2010;27:1093-104.
32. Zhu Y, Stevens RG, Hoffman AE, et al. Epigenetic impact of longterm shiftwork: pilot evidence from circadian genes and wholegenome methylation analysis. Chronobiol Int. 2011;28:852-61.
33. Shi F, Chen X, Fu A, et al. Aberrant DNA methylation of miR-219 promoter in long-term night shiftworkers. Environ Mol Mutagen. 2013;54:406-13.
34. Jacobs DI, Hansen J, Fu A, et al. Methylation alterations at imprinted genes detected among long-term shiftworkers. Environ Mol Mutagen. 2013;54:141-6.
35. Kim J, Bhattacharjee R, Khalyfa A, et al. DNA methylation in inflammatory genes among children with obstructive sleep apnea. Am J Respir Crit Care Med. 2012;185:330-8.
36. Rotter A, Asemann R, Decker A, et al. Orexin expression and promoter-methylation in peripheral blood of patients suffering from major depressive disorder. J Affect Disord. 2011;131:186-92.
37. Lin Q, Ding H, Zheng Z, et al. Promoter methylation analysis of seven clock genes in Parkinson's disease. Neurosci Lett. 2012;507:147-50.
38. Liu HC, Hu CJ, Tang YC, Chang JG. A pilot study for circadian gene disturbance in dementia patients. Neurosci Lett. 2008;435:229-33.
39. •• Hirayama J, Sahar S, Grimaldi B, et al. CLOCK-mediated acetylation of BMAL1 controls circadian function. Nature. 2007;450: 1086-90. This study revealed that the CLOCK protein serves as a histone acetyltransferase enzyme and that this activity plays a role in mediating circadian gene expression. (Pubitemid 350273614)
40. Etchegaray JP, Lee C, Wade PA, Reppert SM. Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature. 2003;421:177-82. (Pubitemid 36090986)
41. • Valekunja UK, Edgar RS, Oklejewicz M, et al. Histone methyltransferase MLL3 contributes to genome-scale circadian transcription. Proc Natl Acad Sci U S A. 2013;110:1554-9. This analysis showed that the expression and function of the mixed lineage leukemia 3, a histone-modifying enzyme, is controlled by the circadian clock and is involved in regulating rhythmic gene expression on a genome-wide scale.
42. Katada S, Sassone-Corsi P. The histone methyltransferase MLL1 permits the oscillation of circadian gene expression. Nat Struct Mol Biol. 2010;17:1414-21.
43. DiTacchio L, Le HD, Vollmers C, et al. Histone lysine demethylase JARID1a activates CLOCK-BMAL1 and influences the circadian clock. Science. 2011;333:1881-5.
44. Cha J, Zhou M, Liu Y. CATP is a critical component of the Neurospora circadian clock by regulating the nucleosome occupancy rhythm at the frequency locus. EMBO Rep. 2013;14:923 -30.
45. • Nakahata Y, Kaluzova M, Grimaldi B, et al. The NAD + -dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell. 2008;134:329-40. This paper reported that NAD + -dependent sirtuin 1 is a histone deacetylase, which is involved in regulating circadian gene expression, and whose enzymatic activity is, both, dependent on cellular metabolic state and subject to circadian regulation.
46. Asher G, Gatfield D, Stratmann M, et al. SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell. 2008;134:317-28. (Pubitemid 352024391)
47. Nakahata Y, Sahar S, Astarita G, et al. Circadian control of the NA + salvage pathway by CLOCK-SIRT1. Science. 2009;324:654-7.
48. Ramsey KM, Yoshino J, Brace CS, et al. Circadian clock feedback cycle through NAMPT-mediated NAD + biosynthesis. Science. 2009;324:651-4.
49. Singh N, Lorbeck MT, Zervos A, et al. The histone acetyltransferase Elp3 plays in active role in the control of synaptic bouton expansion and sleep in Drosophila. J Neurochem. 2010;115:493-504.
50. Pirooznia SK, Chiu K, Chan MT, et al. Epigenetic regulation of axonal growth of Drosophila pacemaker cells by histone acetyltransferase tip60 controls sleep. Genetics. 2012;192:1327-45.
51. Gottlieb DJ, O'Connor GT, Wilk JB. Genome-wide association of sleep and circadian phenotypes. BMC Med Genet. 2007;8 Suppl 1:S9.
52. Kleefstra T, Smidt M, Banning MJ, et al. Disruption of the gene Euchromatin Histone Methyl Transferase1 (Eu-HMTase1) is associated with the 9q34 subtelomeric deletion syndrome. JMed Genet. 2005;42:299-306. (Pubitemid 40523951)
53. Kleefstra T, Brunner HG, Amiel J, et al. Loss-of-function mutations in euchromatin histone methyl transferase 1 (EHMT1) cause the 9q34 subtelomeric deletion syndrome. Am J Hum Genet. 2006;79:370-7. (Pubitemid 44141836)
54. Verhoeven WM, Kleefstra T, Egger JI. Behavioral phenotype in the 9q subtelomeric deletion syndrome: a report about two adult patients. Am J Med Genet B Neuropsychiatr Genet. 2010;153B:536-41.
55. Williams SR, Aldred MA, Der Kaloustian VM, et al. Haploinsufficiency of HDAC4 causes brachydactyly mental retardation syndrome, with brachydactyly type E, developmental delays, and behavioral problems. Am J Hum Genet. 2010;87:219-28.
56. Villavicencio-Lorini P, Klopocki E, Trimborn M, et al. Phenotypic variant of Brachydactyly-mental retardation syndrome in a family with an inherited interstitial 2q37.3 microdeletion including HDAC4. Eur J Hum Genet. 2013;21:743-8.
57. Williams SR, Zies D, Mullegama SV, et al. Smith-Magenis syndrome results in disruption of CLOCK gene transcription and reveals an integral role for RAI1 in the maintenance of circadian rhythmicity. Am J Hum Genet. 2012;90:941-9.
58. • Deardorff MA, Bando M, Nakato R, et al. HDAC8 mutations in Cornelia de Lange syndrome affect the cohesin acetylation cycle. Nature. 2012;489:313-7. This investigation identified loss-of-function mutations in the histone deacetylase 8 gene that deregulate the cohesin complex and are responsible for causing Cornelia de Lange syndrome.
59. Rajan R, Benke JR, Kline AD, et al. Insomnia in Cornelia de Lange syndrome. Int J Pediatr Otorhinolaryngol. 2012;76:972-5.
60. Stavinoha RC, Kline AD, Levy HP, et al. Characterization of sleep disturbance in Cornelia de Lange Syndrome. Int J Pediatr Otorhinolaryngol. 2011;75:215-8.
61. Askarian-Amiri ME, Crawford J, French JD, et al. SNORD-host RNA Zfas1 is a regulator of mammary development and a potential marker for breast cancer. RNA. 2011;17:878-91.
62. Clokie SJ, Lau P, Kim HH, et al. MicroRNAs in the pineal gland: miR-483 regulates melatonin synthesis by targeting arylalkylamine N-acetyltransferase. J Biol Chem. 2012;287:25312-24.
63. Xu S, Witmer PD, Lumayag S, et al. MicroRNA (miRNA) transcriptome of mouse retina and identification of a sensory organ-specific miRNA cluster. J Biol Chem. 2007;282:25053-66. (Pubitemid 47347506)
64. Sire C, Moreno AB, Garcia-Chapa M, et al. Diurnal oscillation in the accumulation of Arabidopsis microRNAs, miR167, miR168, miR171 and miR398. FEBS Lett. 2009;583:1039-44.
65. Yang M, Lee JE, Padgett RW, Edery I. Circadian regulation of a limited set of conserved microRNAs in Drosophila. BMC Genomics. 2008;9:83.
66. Vodala S, Pescatore S, Rodriguez J, et al. The oscillating miRNA 959-964 cluster impacts Drosophila feeding time and other circadian outputs. Cell Metab. 2012;16:601-12.
67. 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. (Pubitemid 47077578)
68. 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.
69. •• Cheng HY, Papp JW, Varlamova O, et al. microRNA modulation of circadian-clock period and entrainment. Neuron. 2007;54: 813-29. This paper provided the first, robust mechanistic evidence that environmentally responsive microRNA activity is involved in the circadian clock within the suprachiasmatic nucleus. (Pubitemid 46843524)
70. Gatfield D, Le Martelot G, Vejnar CE, et al. Integration of microRNA miR-122 in hepatic circadian gene expression. Genes Dev. 2009;23:1313-26.
71. Na YJ, Sung JH, Lee SC, et al. Comprehensive analysis of microRNA-mRNA co-expression in circadian rhythm. Exp Mol Med. 2009;41:638-47.
72. Kadener S, Menet JS, Sugino K, et al. A role for microRNAs in the Drosophila circadian clock. Genes Dev. 2009;23:2179-91.
73. 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.
74. Shende VR, Goldrick MM, Ramani S, Earnest DJ. Expression and rhythmic modulation of circulating microRNAs targeting the clock gene Bmal1 in mice. PLoS One. 2011;6:e22586.
75. Alvarez-Saavedra M, Antoun G, Yanagiya A, et al. miRNA-132 orchestrates chromatin remodeling and translational control of the circadian clock. Hum Mol Genet. 2011;20:731-51.
76. Zhang Y, Emery P. GW182 controls Drosophila circadian behavior and PDF-receptor signaling. Neuron. 2013;78:152-65.
77. Lee KH, Kim SH, Lee HR, et al. MicroRNA-185 oscillation controls circadian amplitude of mouse Cryptochrome 1 via translational regulation. Mol Biol Cell. 2013;24:2248-55.
78. 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.
79. • Hughes ME, Grant GR, Paquin C, et al. Deep sequencing the circadian and diurnal transcriptome of Drosophila brain. Genome Res. 2012;22:1266-81. This study performed RNA sequencing of Drosophila brain and identified hundreds of transcripts with circadian expression profiles, including many noncoding RNAs and those that were targets of RNA editing.
80. • Coon SL, Munson PJ, Cherukuri PF, et al. Circadian changes in long noncoding RNAs in the pineal gland. Proc Natl Acad Sci U S A. 2012;109:13319-24. This investigation of long noncoding RNA profiles in the rat pineal gland found diurnal expression patterns for 112 transcripts that were responsive to light exposure and regulated by norepinephrine signaling from the suprachiasmatic nucleus.
81. Menet JS, Rodriguez J, Abruzzi KC, Rosbash M. Nascent-Seq reveals novel features ofmouse circadian transcriptional regulation. ELife. 2012;1:e00011.
82. Davis CJ, Clinton JM, Taishi P, et al. MicroRNA 132 alters sleep and varies with time in brain. J Appl Physiol. 2011;111:665-72.
83. Soshnev AA, Ishimoto H, McAllister BF, et al. A conserved long noncoding RNA affects sleep behavior in Drosophila. Genetics. 2011;189:455-68.
84. Saus E, Soria V, Escaramis G, 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.
85. .• Powell WT, Coulson RL, Crary FK, et al. A Prader-Willi locus lncRNA cloud modulates diurnal genes and energy expenditure. Hum Mol Genet. 2013;22:4318-28. This analysis of the 116HG long noncoding RNA encoded by the imprinted Prader-Willi locus suggested that this factor is involved in transcriptional regulation of key metabolic and clock genes, in postnatal neurons and during sleep, via the formation of a novel subnuclear domain.
86. Jepson JE, Savva YA, Yokose C, et al. Engineered alterations in RNA editing modulate complex behavior in Drosophila: regulatory diversity of adenosine deaminase acting on RNA (ADAR) targets. J Biol Chem. 2011;286:8325-37.
87. • Fustin JM, Doi M, Yamaguchi Y, et al. RNA-methylation-dependent RNA processing controls the speed of the circadian clock. Cell. 2013;155:793-806. This paper demonstrated that post-transcriptional RNA methylation is a novel component of the circadian clock responsible for targeting core clock transcripts and thereby regulating the length of the circadian period.
88. Qureshi IA, Mehler MF. Towards a 'systems'-level understanding of the nervous system and its disorders. Trends Neurosci. 2013;36:674-84.