The genome-wide landscape of DNA methylation and hydroxymethylation in response to sleep deprivation impacts on synaptic plasticity genes

Translational Psychiatry

Volumn 4, Issue , 2014, Pages

  Massart, R ^a   Freyburger, M ^b,c   Suderman, M ^a   Paquet, J ^c   El Helou, J ^c   Belanger Nelson, E ^c   Rachalski, A ^c   Koumar, O C ^c   Carrier, J ^b,c   Szyf, M ^a,d   Mongrain, V ^b,c  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c HÔPITAL DU SACRÉ COEUR DE MONTRÉAL   (Canada)

^d CANADIAN INSTITUTE FOR ADVANCED RESEARCH   (Canada)

Author keywords

Cortical synchrony; DNA methylation and hydroxylation; Sleep need; Transcription

Indexed keywords

NEUROLIGIN 1; TRANSCRIPTOME; NERVE CELL ADHESION MOLECULE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; BRAIN FUNCTION; CONTROLLED STUDY; CYTOSKELETON; DNA METHYLATION; ELECTROENCEPHALOGRAM; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENETIC ASSOCIATION; LANDSCAPE; MALE; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; REM SLEEP; SIGNAL TRANSDUCTION; SLEEP DEPRIVATION; ANIMAL; C57BL MOUSE; ELECTROENCEPHALOGRAPHY; GENETIC EPIGENESIS; GENETICS; GENOME; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SLEEP STAGE; ANIMAL MODEL; ANIMAL TISSUE; EPIGENETICS; FEAR; NERVE CELL; NEUROPROTECTION;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CEREBRAL CORTEX; DNA METHYLATION; ELECTROENCEPHALOGRAPHY; EPIGENESIS, GENETIC; GENOME; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONAL PLASTICITY; SLEEP DEPRIVATION; SLEEP STAGES; TRANSCRIPTOME;

EID: 84892983160     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2013.120     Document Type: Article

References (68)

1. Boland EM, Alloy LB.. Sleep disturbance and cognitive deficits in bipolar disorder: toward an integrated examination of disorder maintenance and functional impairment. Clin Psychol Rev 2013; 33: 33-44.
2. Krystal AD. Psychiatric disorders and sleep. Neurol Clin 2012; 30: 1389-1413.
3. Kotagal S, Broomall E. Sleep in children with autism spectrum disorder. Pediatr Neurol 2012; 47: 242-251.
4. Hatfield CF, Herbert J, van Someren EJ, Hodges JR, Hastings MH. Disrupted daily activity/rest cycles in relation to daily cortisol rhythms of home-dwelling patients with early Alzheimer's dementia. Brain 2004; 127(Pt 5): 1061-1074. (Pubitemid 38623042)
5. McCoy JG, Strecker RE. The cognitive cost of sleep lost. Neurobiol Learn Mem 2011; 96: 564-582.
6. Walker MP. Cognitive consequences of sleep and sleep loss. Sleep Med 2008; 9 (Suppl 1): S29-S34.
7. Dallaspezia S, Benedetti F. Chronobiological therapy for mood disorders. Expert Rev Neurother 2011; 11: 961-970.
8. Borbély AA. A two process model of sleep regulation. Hum Neurobiol 1982; 1: 195-204. (Pubitemid 13213853)
9. Tononi G, Cirelli C. Sleep function and synaptic homeostasis. Sleep Med Rev 2006; 10: 49-62. (Pubitemid 43106851)
10. Franken P, Dijk DJ. Circadian clock genes and sleep homeostasis. Eur J Neurosci 2009; 29: 1820-1829.
11. Vyazovskiy VV, Olcese U, Lazimy YM, Faraguna U, Esser SK, Williams JC et al. Cortical firing and sleep homeostasis. Neuron 2009; 63: 865-878.
12. Carrier J, Viens I, Poirier G, Robillard R, Lafortune M, Vandewalle G et al. Sleep slow wave changes during the middle years of life. Eur J Neurosci 2011; 33: 758-766.
13. Mongrain V, Carrier J, Paquet J, Bélanger-Nelson E, Dumont M. Morning and evening-type differences in slow waves during NREM sleep reveal both trait and state-dependent phenotypes. PLoS ONE 2011; 6: e22679.
14. Cirelli C, Tononi G. Gene expression in the brain across the sleep-waking cycle. Brain Res 2000; 885: 303-321.
15. 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: 441-457. (Pubitemid 350127784)
16. 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 USA 2007; 104: 20090-20095.
17. 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: 1147-1157.
18. El Helou J, Belanger-Nelson E, Freyburger M, Dorsaz S, Curie T, La Spada F et al. Neuroligin-1 links neuronal activity to sleep-wake regulation. Proc Natl Acad Sci USA 2013; 110: 9974-9979.
19. Sudhof TC. Neuroligins and neurexins link synaptic function to cognitive disease. Nature 2008; 455: 903-911.
20. Daoust AM, Limoges E, Bolduc C, Mottron L, Godbout R. EEG spectral analysis of wakefulness and REM sleep in high functioning autistic spectrum disorders. Clin Neurophysiol 2004; 115: 1368-1373. (Pubitemid 38596721)
21. Munoz PC, Aspe MA, Contreras LS, Palacios AG. Correlations of recognition memory performance with expression and methylation of brain-derived neurotrophic factor in rats. Biol Res 2010; 43: 251-258.
22. Guo JU, Ma DK, Mo H, Ball MP, Jang MH, Bonaguidi MA et al. Neuronal activity modifies the DNA methylation landscape in the adult brain. Nature Neurosci 2011; 14: 1345-1351.
23. Rajasethupathy P, Antonov I, Sheridan R, Frey S, Sander C, Tuschl T et al. A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell 2012; 149: 693-707.
24. Varoqueaux F, Aramuni G, Rawson RL, Mohrmann R, Missler M, Gottmann K et al. Neuroligins determine synapse maturation and function. Neuron 2006; 51: 741-754. (Pubitemid 44374915)
25. Franken P, Dijk DJ, Tobler I, Borbély AA. Sleep deprivation in rats: effects on EEG power spectra, vigilance states, and cortical temperature. Am J Physiol 1991; 261 (Pt 2): R198-R208.
26. Franken P, Malafosse A, Tafti M. Genetic variation in EEG activity during sleep in inbred mice. Am J Physiol 1998; 275(Pt 2): R1127-R1137.
27. Mölle M, Yeshenko O, Marshall L, Sara SJ, Born J. Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J Neurophysiol 2006; 96: 62-70. (Pubitemid 44015342)
28. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Statist Soc Ser B 1995; 57: 289-300.
29. Provencal N, Suderman MJ, Guillemin C, Massart R, Ruggiero A, Wang D et al. The signature of maternal rearing in the methylome in rhesus macaque prefrontal cortex and T cells. J Neurosci 2012; 32: 15626-15642.
30. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4: 44-57.
31. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009; 37: 1-13.
32. Esser SK, Hill SL, Tononi G. Sleep homeostasis and cortical synchronization: I. Modeling the effects of synaptic strength on sleep slow waves. Sleep 2007; 30: 1617-1630. (Pubitemid 350234741)
33. Brown SJ, Stoilov P, Xing Y. Chromatin and epigenetic regulation of pre-mRNA processing. Hum Mol Genet 2012; 21: R90-R96.
34. Valinluck V, Tsai HH, Rogstad DK, Burdzy A, Bird A, Sowers LC. Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Res 2004; 32: 4100-4108. (Pubitemid 39232282)
35. Donohoe DR, Bultman SJ. Metaboloepigenetics: interrelationships between energy metabolism and epigenetic control of gene expression. J Cell Physiol 2012; 227: 3169-3177.
36. Aguilar-Arnal L, Sassone-Corsi P. The circadian epigenome: how metabolism talks to chromatin remodeling. Curr Opin Cell Biol 2013; 25: 170-176.
37. Runkel F, Rohlmann A, Reissner C, Brand SM, Missler M. Promoter-like sequences regulating transcriptional activity in neurexin and neuroligin genes. J Neurochem 2013; 127: 36-47.
38. Tammen SA, Friso S, Choi SW. Epigenetics: the link between nature and nurture. Mol Aspects Med 2013; 34: 753-764.
39. Szyf M, McGowan P, Meaney MJ. The social environment and the epigenome. Environ Mol Mutagen 2008; 49: 46-60. (Pubitemid 351297595)
40. Zovkic IB, Guzman-Karlsson MC, Sweatt JD. Epigenetic regulation of memory formation and maintenance. Learn Mem 2013; 20: 61-74.
41. Kriaucionis S, Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009; 324: 929-930.
42. Szulwach KE, Li X, Li Y, Song CX, Wu H, Dai Q et al. 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat Neurosci 2011; 14: 1607-1616.
43. Jin SG, Wu X, Li AX, Pfeifer GP. Genomic mapping of 5- hydroxymethylcytosine in the human brain. Nucleic Acids Res 2011; 39: 5015-5024.
44. Hashimoto H, Liu Y, Upadhyay AK, Chang Y, Howerton SB, Vertino PM et al. Recognition and potential mechanisms for replication and erasure of cytosine hydroxymethylation. Nucleic Acids Res 2012; 40: 4841-4849.
45. Yildirim O, Li R, Hung JH, Chen PB, Dong X, Ee LS et al. Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells. Cell 2011; 147: 1498-1510.
46. Song CX, Szulwach KE, Fu Y, Dai Q, Yi C, Li X et al. Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat Biotechnol 2011; 29: 68-72.
47. Varela-Nallar L, Parodi J, Farias GG, Inestrosa NC. Wnt-5a is a synaptogenic factor with neuroprotective properties against Abeta toxicity. Neurodegener Dis 2012; 10: 23-26.
48. Khvotchev MV, Ren M, Takamori S, Jahn R, Südhof TC. Divergent functions of neuronal Rab11b in Ca2+-regulated versus constitutive exocytosis. J Neurosci 2003; 23: 10531-10539. (Pubitemid 37485266)
49. Redies C, Hertel N, Hubner CA. Cadherins and neuropsychiatric disorders. Brain Res 2012; 1470: 130-144.
50. Vardimon L, Kressmann A, Cedar H, Maechler M, Doerfler W. Expression of a cloned adenovirus gene is inhibited by in vitro methylation. Proc Natl Acad Sci USA 1982; 79: 1073-1077. (Pubitemid 12114067)
51. Kulis M, Queirós AC, Beekman R, Martín-Subero JI. Intragenic DNA methylation in transcriptional regulation, normal differentiation and cancer. Biochim Biophys Acta 2013; S1874-9399: 00122-00123.
52. Day JJ, Childs D, Guzman-Karlsson MC, Kibe M, Moulden J, Song E et al. DNA methylation regulates associative reward learning. Nat Neurosci 2013; 16: 1445-1452.
53. Chubykin AA, Atasoy D, Etherton MR, Brose N, Kavalali ET, Gibson JR et al. Activitydependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 2007; 54: 919-931. (Pubitemid 46907504)
54. Peixoto RT, Kunz PA, Kwon H, Mabb AM, Sabatini BL, Philpot BD et al. Transsynaptic signaling by activity-dependent cleavage of neuroligin-1. Neuron 2012; 76: 396-409.
55. De Saint Hilaire Z, Nicolaïdis S. Enhancement of slow wave sleep parallel to the satiating effect of acidic fibroblast growth factor in rats. Brain Res Bull 1992; 29: 525-528.
56. Galan JM, Cuevas B, Dujovny N, Giménez-Gallego G, Cuevas P. Sleep promoting effects of intravenously administered acidic fibroblast growth factor. Neurol Res 1996; 18: 567-569. (Pubitemid 27009395)
57. Bellesi M, Pfister-Genskow M, Maret S, Keles S, Tononi G, Cirelli C. Effects of sleep and wake on oligodendrocytes and their precursors. J Neurosci 2013; 33: 14288-14300.
58. Oliveira AM, Hemstedt TJ, Bading H. Rescue of aging-associated decline in Dnmt3a2 expression restores cognitive abilities. Nat Neurosci 2012; 15: 1111-1113.
59. Igarashi K, Katoh Y. Metabolic aspects of epigenome: coupling of s-adenosylmethionine synthesis and gene regulation on chromatin by SAMIT module. Subcell Biochem 2012; 61: 105-118.
60. Miller CA, Campbell SL, Sweatt JD. DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity. Neurobiol Learn Mem 2008; 89: 599-603. (Pubitemid 351484241)
61. Lubin FD, Roth TL, Sweatt JD. Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J Neurosci 2008; 28: 10576-10586.
62. van Vliet J, Oates NA, Whitelaw E. Epigenetic mechanisms in the context of complex diseases. Cell Mol Life Sci 2007; 64: 1531-1538. (Pubitemid 46954151)
63. Metivier R, Gallais R, Tiffoche C, Le Peron C, Jurkowska RZ, Carmouche RP et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008; 452: 45-50. (Pubitemid 351355084)
64. Kangaspeska S, Stride B, Metivier R, Polycarpou-Schwarz M, Ibberson D, Carmouche RP et al. Transient cyclical methylation of promoter DNA. Nature 2008; 452: 112-115. (Pubitemid 351355094)
65. Trenell MI, Marshall NS, Rogers NL. Sleep and metabolic control: waking to a problem? Clin Exp Pharmacol Physiol 2007; 34: 1-9. (Pubitemid 46069578)
66. Kultz D. Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol 2005; 67: 225-257. (Pubitemid 40404492)
67. Krueger DD, Tuffy LP, Papadopoulos T, Brose N. The role of neurexins and neuroligins in the formation, maturation, and function of vertebrate synapses. Curr Opin Neurobiol 2012; 22: 412-422.
68. Szyf M. The early-life social environment and DNA methylation. Clin Genet 2012; 81: 341-349.