DNA Methylation Mediates Persistent Epileptiform Activity In Vitro and In Vivo

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Machnes, Ziv M ^a   Huang, Tony C T ^a   Chang, Philip K Y ^a   Gill, Raminder ^a   Reist, Nicholas ^a   Dezsi, Gabriella ^b   Ozturk, Ezgi ^b   Charron, Francois ^a   O'Brien, Terence J ^b   Jones, Nigel C ^b   McKinney, R Anne ^a   Szyf, Moshe ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; DIAZEPAM; GLUTAMATE RECEPTOR 2; KAINIC ACID; MESSENGER RNA; N PHTHALOYLTRYPTOPHAN;

5' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DNA METHYLATION; DOWN REGULATION; EPILEPSY; EPILEPTIC DISCHARGE; EPILEPTIC STATE; GENE; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GRIA2 GENE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN FUNCTION; RAT;

5' FLANKING REGION; ANIMALS; CELL LINE; CPG ISLANDS; DNA METHYLATION; EPILEPSY; GENE ORDER; GENETIC ASSOCIATION STUDIES; HIPPOCAMPUS; HUMANS; KAINIC ACID; MALE; MEMBRANE POTENTIALS; MICE; NEURONS; PHENOTYPE; PHTHALIMIDES; PROMOTER REGIONS, GENETIC; RATS; RECEPTORS, AMPA; SEIZURES; TRYPTOPHAN;

EID: 84884846171     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076299     Document Type: Article

References (57)

1. Razin A, (1998) CpG methylation, chromatin structure and gene silencing-a three-way connection. EMBO J 17: 4905-4908. doi:10.1093/emboj/17.17.4905. PubMed: 9724627.
2. Szyf M, (2009) Epigenetics, DNA Methylation, and Chromatin Modifying Drugs. Annu Rev Pharmacol Toxicol 49: 243-263. doi:10.1146/annurev-pharmtox-061008-103102. PubMed: 18851683.
3. Zachariah RM, Rastegar M, (2012) Linking epigenetics to human disease and Rett syndrome: the emerging novel and challenging concepts in MeCP2 research. Neural Plast,(2012): pp. 415825. PubMed: 22474603.
4. Portela A, Liz J, Nogales V, Setién F, Villanueva A, et al. (2013) DNA methylation determines nucleosome occupancy in the 5'-CpG islands of tumor suppressor genes. Oncogene. PubMed: 23686312.
5. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, et al. (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7: 847-854. doi:10.1038/nn1276. PubMed: 15220929.
6. Szyf M, (2011) The early life social environment and DNA methylation: DNA methylation mediating the long-term impact of social environments early in life. Epigenetics 6: 971-978. doi:10.4161/epi.6.8.16793. PubMed: 21772123.
7. Nelson ED, Kavalali ET, Monteggia LM, (2008) Activity-Dependent Suppression of Miniature Neurotransmission through the Regulation of DNA Methylation. J Neurosci 28: 395-406. doi:10.1523/JNEUROSCI.3796-07.2008. PubMed: 18184782.
8. Levenson JM, Roth TL, Lubin FD, Miller CA, Huang IC, et al. (2006) Evidence That DNA (Cytosine-5) Methyltransferase Regulates Synaptic Plasticity in the Hippocampus. J Biol Chem 281: 15763-15773. doi:10.1074/jbc.M511767200. PubMed: 16606618.
9. Qureshi IA, Mehler MF, (2010) Epigenetic mechanisms underlying human epileptic disorders and the process of epileptogenesis. Neurobiol Dis 39: 53-60. doi:10.1016/j.nbd.2010.02.005. PubMed: 20188170.
10. Kobow K, Blümcke I, (2011) The methylation hypothesis: Do epigenetic chromatin modifications play a role in epileptogenesis? Epilepsia 52: 15-19. doi:10.1111/j.1528-1167.2011.03145.x. PubMed: 21732935.
11. Kobow K, Auvin S, Jensen F, Löscher W, Mody I, et al. (2012) Finding a better drug for epilepsy: Antiepileptogenesis targets. Epilepsia 53: 1868-1876. doi:10.1111/j.1528-1167.2012.03716.x. PubMed: 23061663.
12. Kobow K, Jeske I, Hildebrandt M, Hauke J, Hahnen E, et al. (2009) Increased Reelin Promoter Methylation Is Associated With Granule Cell Dispersion in Human Temporal Lobe Epilepsy. J Neuropathol Exp Neurol 68: 356-364. doi:10.1097/NEN.0b013e31819ba737. PubMed: 19287316.
13. Phiel CJ, Zhang F, Huang EY, Guenther MG, Lazar MA, et al. (2001) Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 276: 36734-36741. doi:10.1074/jbc.M101287200. PubMed: 11473107.
14. Detich N, Bovenzi V, Szyf M, (2003) Valproate induces replication-independent active DNA demethylation. J Biol Chem 278: 27586-27592. doi:10.1074/jbc.M303740200. PubMed: 12748177.
15. Milutinovic S, D'Alessio AC, Detich N, Szyf M, (2007) Valproate induces widespread epigenetic reprogramming which involves demethylation of specific genes. Carcinogenesis 28: 560-571. PubMed: 17012225.
16. Dong E, Guidotti A, Grayson DR, Costa E, (2007) Histone hyperacetylation induces demethylation of reelin and 67-kDa glutamic acid decarboxylase promoters. Proc Natl Acad Sci U S A 104: 4676-4681. doi:10.1073/pnas.0700529104. PubMed: 17360583.
17. Miller-Delaney SF, Das S, Sano T, Jimenez-Mateos EM, Bryan K, et al. (2012) Differential DNA methylation patterns define status epilepticus and epileptic tolerance. J Neurosci 32: 1577-1588. doi:10.1523/JNEUROSCI.5180-11.2012. PubMed: 22302800.
18. Friedman LK, Pellegrini-Giampietro DE, Sperber EF, Bennett MV, Moshé SL, et al. (1994) Kainate-induced status epilepticus alters glutamate and GABAA receptor gene expression in adult rat hippocampus: an in situ hybridization study. J Neurosci 14: 2697-2707. PubMed: 8182436.
19. Pellegrini-Giampietro DE, Gorter JA, Bennett MV, Zukin RS, (1997) The GluR2 (GluR-B) hypothesis: Ca(2+)-permeable AMPA receptors in neurological disorders. Trends Neurosci 20: 464-470. doi:10.1016/S0166-2236(97)01100-4. PubMed: 9347614.
20. Tanaka H, Grooms SY, Bennett MV, Zukin RS, (2000) The AMPAR subunit GluR2: still front and center-stage. Brain Res 886: 190-207. doi:10.1016/S0006-8993(00)02951-6. PubMed: 11119696.
21. Scharfman HE, Gray WP, (2007) Relevance of seizure-induced neurogenesis in animal models of epilepsy to the etiology of temporal lobe epilepsy. Epilepsia 48 (Suppl 2):: 33-41. doi:10.1111/j.1528-1167.2007.01065.x. PubMed: 17571351.
22. Friedman LK, Koudinov AR, (1999) Unilateral GluR2(B) hippocampal knockdown: a novel partial seizure model in the developing rat. J Neurosci 19: 9412-9425. PubMed: 10531445.
23. Huang Y, Doherty JJ, Dingledine R, (2002) Altered histone acetylation at glutamate receptor 2 and brain-derived neurotrophic factor genes is an early event triggered by status epilepticus. J Neurosci 22: 8422-8428. PubMed: 12351716.
24. Brueckner B, Boy RG, Siedlecki P, Musch T, Kliem HC, et al. (2005) Epigenetic reactivation of tumor suppressor genes by a novel small-molecule inhibitor of human DNA methyltransferases. Cancer Res 65: 6305-6311. doi:10.1158/0008-5472.CAN-04-2957. PubMed: 16024632.
25. Gähwiler BH, Capogna M, Debanne D, McKinney RA, Thompson SM, (1997) Organotypic slice cultures: a technique has come of age. Trends Neurosci 20: 471-477. doi:10.1016/S0166-2236(97)01122-3. PubMed: 9347615.
26. Farré D, Roset R, Huerta M, Adsuara JE, Roselló L, et al. (2003) Identification of patterns in biological sequences at the ALGGEN server: PROMO and MALGEN. Nucleic Acids Res 31: 3651-3653. doi:10.1093/nar/gkg605. PubMed: 12824386.
27. Patel A, Bulloch K, (2003) Type II glucocorticoid receptor immunoreactivity in the mossy cells of the rat and the mouse hippocampus. Hippocampus 13: 59-66. doi:10.1002/hipo.10045. PubMed: 12625458.
28. Bao GS, Cheng XQ, Hua Y, Wang ZD, Liu ZG, (2011) Changes of glucocorticoid receptor mRNA expression in basolateral amygdale-kindled rats. Chin Med J (Engl) 124: 2622-2627. PubMed: 22040414.
29. French JA, Williamson PD, Thadani VM, Darcey TM, Mattson RH, et al. (1993) Characteristics of medial temporal lobe epilepsy: I. Results of history and physical examination. Ann Neurol 34: 774-780. doi:10.1002/ana.410340604. PubMed: 8250525.
30. Pernot F, Dorandeu F, Beaup C, Peinnequin A, (2010) Selection of reference genes for real-time quantitative reverse transcription-polymerase chain reaction in hippocampal structure in a murine model of temporal lobe epilepsy with focal seizures. J Neurosci Res 88: 1000-1008. PubMed: 19937810.
31. Wierschke S, Gigout S, Horn P, Lehmann TN, Dehnicke C, et al. (2010) Evaluating reference genes to normalize gene expression in human epileptogenic brain tissues. Biochem Biophys Res Commun 403: 385-390. doi:10.1016/j.bbrc.2010.10.138. PubMed: 21081112.
32. Grooms SY, Opitz T, Bennett MVL, Zukin RS, (2000) Status epilepticus decreases glutamate receptor 2 mRNA and protein expression in hippocampal pyramidal cells before neuronal death. Proc Natl Acad Sci U S A 97: 3631-3636. doi:10.1073/pnas.97.7.3631. PubMed: 10725374.
33. Routbort MJ, Bausch SB, McNamara JO, (1999) Seizures, cell death, and mossy fiber sprouting in kainic acid-treated organotypic hippocampal cultures. Neuroscience 94: 755-765. doi:10.1016/S0306-4522(99)00358-9. PubMed: 10579566.
34. Holopainen IE, Järvelä J, Lopez-Picon FR, Pelliniemi LJ, Kukko-Lukjanov TK, (2004) Mechanisms of kainate-induced region-specific neuronal death in immature organotypic hippocampal slice cultures. Neurochem Int 45: 1-10. doi:10.1016/j.neuint.2004.01.005. PubMed: 15082216.
35. Myers SJ, Peters J, Huang Y, Comer MB, Barthel F, et al. (1998) Transcriptional Regulation of the GluR2 Gene: Neural-Specific Expression, Multiple Promoters, and Regulatory Elements. J Neurosci 18: 6723-6739. PubMed: 9712644.
36. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, et al. (2010) Glutamate Receptor Ion Channels: Structure, Regulation, and Function. Pharmacol Rev 62: 405-496. doi:10.1124/pr.109.002451. PubMed: 20716669.
37. Klug M, Rehli M, (2006) Functional analysis of promoter CpG methylation using a CpG-free luciferase reporter vector. Epigenetics 1: 127-130. doi:10.4161/epi.1.3.3327. PubMed: 17965610.
38. Xi ZQ, Xiao F, Yuan J, Wang XF, Wang L, et al. (2009) Gene expression analysis on anterior temporal neocortex of patients with intractable epilepsy. Synapse 63: 1017-1028. doi:10.1002/syn.20681. PubMed: 19623530.
39. Jamali S, Bartolomei F, Robaglia-Schlupp A, Massacrier A, Peragut JC, et al. (2006) Large-scale expression study of human mesial temporal lobe epilepsy: evidence for dysregulation of the neurotransmission and complement systems in the entorhinal cortex. Brain 129: 625-641. doi:10.1093/brain/awl001. PubMed: 16399808.
40. Arion D, Sabatini M, Unger T, Pastor J, Alonso-Nanclares L, et al. (2006) Correlation of transcriptome profile with electrical activity in temporal lobe epilepsy. Neurobiol Dis 22: 374-387. doi:10.1016/j.nbd.2005.12.012. PubMed: 16480884.
41. Suzuki F, Hirai H, Onteniente B, Riban V, Matsuda M, et al. (2000) Long-term increase of GluR2 α-amino-3-hydroxy-5-methylisoxazole-4-propionate receptor subunit in the dispersed dentate gyrus after intrahippocampal kainate injection in the mouse. Neuroscience 101: 41-50. doi:10.1016/S0306-4522(00)00359-6. PubMed: 11068135.
42. Kobow K, Blümcke I, (2012) The emerging role of DNA methylation in epileptogenesis. Epilepsia 53: 11-20. doi:10.1111/epi.12031. PubMed: 23216575.
43. Bell JT, Saffery R, (2012) The value of twins in epigenetic epidemiology. Int J Epidemiol, 41: 140-50. PubMed: 22253312.
44. Bell JT, Spector TD, (2011) A twin approach to unraveling epigenetics. Trends Genet 27: 116-125. doi:10.1016/j.tig.2010.12.005. PubMed: 21257220.
45. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, et al. (2005) Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A 102: 10604-10609. doi:10.1073/pnas.0500398102. PubMed: 16009939.
46. Nguyen A, Rauch TA, Pfeifer GP, Hu VW, (2010) Global methylation profiling of lymphoblastoid cell lines reveals epigenetic contributions to autism spectrum disorders and a novel autism candidate gene, RORA, whose protein product is reduced in autistic brain. FASEB J 24: 3036-3051. doi:10.1096/fj.10-154484. PubMed: 20375269.
47. Kaminsky ZA, Tang T, Wang SC, Ptak C, Oh GH, et al. (2009) DNA methylation profiles in monozygotic and dizygotic twins. Nat Genet 41: 240-245. doi:10.1038/ng.286. PubMed: 19151718.
48. Petronis A, (2006) Epigenetics and twins: three variations on the theme. Trends Genet 22: 347-350. doi:10.1016/j.tig.2006.04.010. PubMed: 16697072.
49. Singh SM, Murphy B, O'Reilly R, (2002) Epigenetic contributors to the discordance of monozygotic twins. Clin Genet 62: 97-103. doi:10.1034/j.1399-0004.2002.620201.x. PubMed: 12220446.
50. Dempster EL, Pidsley R, Schalkwyk LC, Owens S, Georgiades A, et al. (2011) Disease-associated epigenetic changes in monozygotic twins discordant for schizophrenia and bipolar disorder. Hum Mol Genet 20: 4786-4796. doi:10.1093/hmg/ddr416. PubMed: 21908516.
51. Morimoto K, Fahnestock M, Racine RJ, (2004) Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog Neurobiol 73: 1-60. doi:10.1016/j.pneurobio.2004.03.009. PubMed: 15193778.
52. Jupp B, Williams J, Binns D, Hicks RJ, Cardamone L, et al. (2012) Hypometabolism precedes limbic atrophy and spontaneous recurrent seizures in a rat model of TLE. Epilepsia 53: 1233-1244. doi:10.1111/j.1528-1167.2012.03525.x. PubMed: 22686573.
53. Jones NC, Salzberg MR, Kumar G, Couper A, Morris MJ, et al. (2008) Elevated anxiety and depressive-like behavior in a rat model of genetic generalized epilepsy suggesting common causation. Exp Neurol 209: 254-260. doi:10.1016/j.expneurol.2007.09.026. PubMed: 18022621.
54. Li LC, Dahiya R, (2002) MethPrimer: designing primers for methylation PCRs. Bioinformatics 18: 1427-1431. doi:10.1093/bioinformatics/18.11.1427. PubMed: 12424112.
55. Matevossian A, Akbarian S, (2008) Neuronal nuclei isolation from human postmortem brain tissue. J Vis Exp. PubMed: 19078943.
56. Corpet F, (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16: 10881-10890. doi:10.1093/nar/16.22.10881. PubMed: 2849754.
57. Ludbrook J, (1998) MULTIPLE COMPARISON PROCEDURES UPDATED. Clin Exp Pharmacol Physiol 25: 1032-1037. doi:10.1111/j.1440-1681.1998.tb02179.x. PubMed: 9888002.