Epigenetics of schizophrenia: An open and shut case

International Review of Neurobiology

Volumn 115, Issue , 2014, Pages 155-201

  Gavin, David P ^a,b   Floreani, Christina ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

Bipolar disorder; CpG methylation; Demethylation; GADD45; Psychosis

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3F; ARIPIPRAZOLE; AZACITIDINE; BRAIN DERIVED NEUROTROPHIC FACTOR; CLOZAPINE; DNA; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DOPAMINE 2 RECEPTOR BLOCKING AGENT; EPIGALLOCATECHIN GALLATE; HALOPERIDOL; HISTONE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE INHIBITOR; LURASIDONE; NEUROLEPTIC AGENT; PHENELZINE; PIMOZIDE; PROCAINAMIDE; QUETIAPINE; ROMIDEPSIN; SULPIRIDE; TRANSCRIPTION FACTOR SOX10; TRANYLCYPROMINE; TRICHOSTATIN A; UNINDEXED DRUG; VALPROIC ACID; VESICULAR GLUTAMATE TRANSPORTER 1; VORINOSTAT;

ARTICLE; BIPOLAR DISORDER; BLOOD CELL; BRAIN ISCHEMIA; DEMETHYLATION; DISEASE COURSE; DNA METHYLATION; DRUG EFFICACY; DRUG MECHANISM; DRUG TARGETING; EPIGENETICS; EUCHROMATIN; GENE EXPRESSION; GENE SILENCING; HETEROCHROMATIN; HISTONE MODIFICATION; HUMAN; NONHUMAN; PATHOPHYSIOLOGY; PERSONALIZED MEDICINE; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROMOTER REGION; SCHIZOPHRENIA; ANIMAL; CPG ISLAND; GENETIC EPIGENESIS; GENETICS; PHYSIOLOGY;

ANIMALS; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; HUMANS; SCHIZOPHRENIA;

EID: 84905962153     PISSN: 00747742     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-801311-3.00005-6     Document Type: Chapter

References (244)

1. Abdolmaleky H.M., Cheng K.H., Faraone S.V., Wilcox M., Glatt S.J., Gao F., et al. Hypomethylation of MB-COMT promoter is a major risk factor for schizophrenia and bipolar disorder. Human Molecular Genetics 2006, 15(21):3132-3145. 10.1093/hmg/ddl253.
2. Abdolmaleky H.M., Cheng K.H., Russo A., Smith C.L., Faraone S.V., Wilcox M., et al. Hypermethylation of the reelin (RELN) promoter in the brain of schizophrenic patients: A preliminary report. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics: the Official Publication of the International Society of Psychiatric Genetics 2005, 134B(1):60-66. 10.1002/ajmg.b.30140.
3. Adams-Cioaba M.A., Min J. Structure and function of histone methylation binding proteins. Biochemistry and Cell Biology: Biochimie et Biologie Cellulaire 2009, 87(1):93-105. 10.1139/O08-129.
4. Agalioti T., Chen G., Thanos D. Deciphering the transcriptional histone acetylation code for a human gene. Cell 2002, 111(3):381-392.
5. Akbarian S., Huang H.S. Epigenetic regulation in human brain-focus on histone lysine methylation. Biological Psychiatry 2009, 65(3):198-203. 10.1016/j.biopsych.2008.08.015.
6. Akbarian S., Ruehl M.G., Bliven E., Luiz L.A., Peranelli A.C., Baker S.P., et al. Chromatin alterations associated with down-regulated metabolic gene expression in the prefrontal cortex of subjects with schizophrenia. Archives of General Psychiatry 2005, 62(8):829-840. 10.1001/archpsyc.62.8.829.
7. Arion D., Unger T., Lewis D.A., Levitt P., Mirnics K. Molecular evidence for increased expression of genes related to immune and chaperone function in the prefrontal cortex in schizophrenia. Biological Psychiatry 2007, 62(7):711-721. 10.1016/j.biopsych.2006.12.021.
8. Arnaudo A.M., Garcia B.A. Proteomic characterization of novel histone post-translational modifications. Epigenetics & Chromatin 2013, 6(1):24. 10.1186/1756-8935-6-24.
9. Attwood J.T., Yung R.L., Richardson B.C. DNA methylation and the regulation of gene transcription. Cellular and Molecular Life Sciences: CMLS 2002, 59(2):241-257.
10. Auta J., Smith R.C., Dong E., Tueting P., Sershen H., Boules S., et al. DNA-methylation gene network dysregulation in peripheral blood lymphocytes of schizophrenia patients. Schizophrenia Research 2013, 150(1):312-318. 10.1016/j.schres.2013.07.030.
11. Bachman K.E., Rountree M.R., Baylin S.B. Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. The Journal of Biological Chemistry 2001, 276(34):32282-32287. 10.1074/jbc.M104661200.
12. Bell J.T., Tsai P.C., Yang T.P., Pidsley R., Nisbet J., Glass D., et al. Epigenome-wide scans identify differentially methylated regions for age and age-related phenotypes in a healthy ageing population. PLoS Genetics 2012, 8(4):e1002629. 10.1371/journal.pgen.1002629.
13. Benes F.M., Lim B., Matzilevich D., Walsh J.P., Subburaju S., Minns M. Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(24):10164-10169. 10.1073/pnas.0703806104.
14. Benes F.M., Lim B., Subburaju S. Site-specific regulation of cell cycle and DNA repair in post-mitotic GABA cells in schizophrenic versus bipolars. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(28):11731-11736. 10.1073/pnas.0903066106.
15. Benten D., Keller G., Quaas A., Schrader J., Gontarewicz A., Balabanov S., et al. Aurora kinase inhibitor PHA-739358 suppresses growth of hepatocellular carcinoma in vitro and in a xenograft mouse model. Neoplasia (New York, NY) 2009, 11(9):934-944.
16. Bestor T.H. The DNA methyltransferases of mammals. Human Molecular Genetics 2000, 9(16):2395-2402.
17. Bhattacharya S.K., Ramchandani S., Cervoni N., Szyf M. A mammalian protein with specific demethylase activity for mCpG DNA. Nature 1999, 397(6720):579-583. 10.1038/17533.
18. Bird A. DNA methylation patterns and epigenetic memory. Genes & Development 2002, 16(1):6-21. 10.1101/gad.947102.
19. Bollati V., Baccarelli A., Hou L., Bonzini M., Fustinoni S., Cavallo D., et al. Changes in DNA methylation patterns in subjects exposed to low-dose benzene. Cancer Research 2007, 67(3):876-880. 10.1158/0008-5472.CAN-06-2995.
20. Bonsch D., Wunschel M., Lenz B., Janssen G., Weisbrod M., Sauer H. Methylation matters? Decreased methylation status of genomic DNA in the blood of schizophrenic twins. Psychiatry Research 2012, 198(3):533-537. 10.1016/j.psychres.2011.09.004.
21. Bredy T.W., Barad M. The histone deacetylase inhibitor valproic acid enhances acquisition, extinction, and reconsolidation of conditioned fear. Learning & Memory (Cold Spring Harbor, NY) 2008, 15(1):39-45. 10.1101/lm.801108.
22. Bredy T.W., Wu H., Crego C., Zellhoefer J., Sun Y.E., Barad M. Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear. Learning & Memory (Cold Spring Harbor, NY) 2007, 14(4):268-276. 10.1101/lm.500907.
23. Brennand K.J., Simone A., Jou J., Gelboin-Burkhart C., Tran N., Sangar S., et al. Modelling schizophrenia using human induced pluripotent stem cells. Nature 2011, 473(7346):221-225. 10.1038/nature09915.
24. Bromberg A., Levine J., Nemetz B., Belmaker R.H., Agam G. No association between global leukocyte DNA methylation and homocysteine levels in schizophrenia patients. Schizophrenia Research 2008, 101(1-3):50-57. 10.1016/j.schres.2008.01.009.
25. Calabrese F., Luoni A., Guidotti G., Racagni G., Fumagalli F., Riva M.A. Modulation of neuronal plasticity following chronic concomitant administration of the novel antipsychotic lurasidone with the mood stabilizer valproic acid. Psychopharmacology 2013, 226(1):101-112. 10.1007/s00213-012-2900-0.
26. Campanero M.R., Herrero A., Calvo V. The histone deacetylase inhibitor trichostatin A induces GADD45 gamma expression via oct and NF-Y binding sites. Oncogene 2008, 27(9):1263-1272. 10.1038/sj.onc.1210735.
27. Canettieri G., Morantte I., Guzman E., Asahara H., Herzig S., Anderson S.D., et al. Attenuation of a phosphorylation-dependent activator by an HDAC-PP1 complex. Nature Structural Biology 2003, 10(3):175-181. 10.1038/nsb895.
28. Carrard A., Salzmann A., Malafosse A., Karege F. Increased DNA methylation status of the serotonin receptor 5HTR1A gene promoter in schizophrenia and bipolar disorder. Journal of Affective Disorders 2011, 132(3):450-453. 10.1016/j.jad.2011.03.018.
29. Carrier F., Georgel P.T., Pourquier P., Blake M., Kontny H.U., Antinore M.J., et al. Gadd45, a p53-responsive stress protein, modifies DNA accessibility on damaged chromatin. Molecular and Cellular Biology 1999, 19(3):1673-1685.
30. Cencioni C., Spallotta F., Martelli F., Valente S., Mai A., Zeiher A.M., et al. Oxidative stress and epigenetic regulation in ageing and age-related diseases. International Journal of Molecular Sciences 2013, 14(9):17643-17663. 10.3390/ijms140917643.
31. Chase K.A., Gavin D.P., Guidotti A., Sharma R.P. Histone methylation at H3K9: Evidence for a restrictive epigenome in schizophrenia. Schizophrenia Research 2013, 149(1-3):15-20. 10.1016/j.schres.2013.06.021.
32. Chen W.G., Chang Q., Lin Y., Meissner A., West A.E., Griffith E.C., et al. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science (New York, NY) 2003, 302(5646):885-889. 10.1126/science.1086446.
33. Chen Z., Clark S., Birkeland M., Sung C.M., Lago A., Liu R., et al. Induction and superinduction of growth arrest and DNA damage gene 45 (GADD45) alpha and beta messenger RNAs by histone deacetylase inhibitors trichostatin A (TSA) and butyrate in SW620 human colon carcinoma cells. Cancer Letters 2002, 188(1-2):127-140.
34. Cheng M.C., Liao D.L., Hsiung C.A., Chen C.Y., Liao Y.C., Chen C.H. Chronic treatment with aripiprazole induces differential gene expression in the rat frontal cortex. The International Journal of Neuropsychopharmacology/Official Scientific Journal of the Collegium Internationale Neuropsychopharmacologicum (CINP) 2008, 11(2):207-216. 10.1017/S1461145707008048.
35. Cheung P., Tanner K.G., Cheung W.L., Sassone-Corsi P., Denu J.M., Allis C.D. Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Molecular Cell 2000, 5(6):905-915.
36. Ciccarone F., Klinger F.G., Catizone A., Calabrese R., Zampieri M., Bacalini M.G., et al. Poly(ADP-ribosyl)ation acts in the DNA demethylation of mouse primordial germ cells also with DNA damage-independent roles. PLoS One 2012, 7(10):e46927. 10.1371/journal.pone.0046927.
37. Ciccone D.N., Su H., Hevi S., Gay F., Lei H., Bajko J., et al. KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints. Nature 2009, 461(7262):415-418. 10.1038/nature08315.
38. Cohen-Armon M., Visochek L., Katzoff A., Levitan D., Susswein A.J., Klein R., et al. Long-term memory requires polyADP-ribosylation. Science (New York, NY) 2004, 304(5678):1820-1822. 10.1126/science.1096775.
39. Cortellino S., Xu J., Sannai M., Moore R., Caretti E., Cigliano A., et al. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 2011, 146(1):67-79. 10.1016/j.cell.2011.06.020.
40. Covington H.E., Maze I., LaPlant Q.C., Vialou V.F., Ohnishi Y.N., Berton O., et al. Antidepressant actions of histone deacetylase inhibitors. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2009, 29(37):11451-11460. 10.1523/JNEUROSCI.1758-09.2009.
41. Creusot F., Acs G., Christman J.K. Inhibition of DNA methyltransferase and induction of friend erythroleukemia cell differentiation by 5-azacytidine and 5-aza-2'-deoxycytidine. The Journal of Biological Chemistry 1982, 257(4):2041-2048.
42. Cuadrado-Tejedor M., Ricobaraza A.L., Torrijo R., Franco R., Garcia-Osta A. Phenylbutyrate is a multifaceted drug that exerts neuroprotective effects and reverses the Alzheimer's disease-like phenotype of a commonly used mouse model. Current Pharmaceutical Design 2013, 19(28):5076-5084.
43. Daigle S.R., Olhava E.J., Therkelsen C.A., Basavapathruni A., Jin L., Boriack-Sjodin P.A., et al. Potent inhibition of DOT1L as treatment of MLL-fusion leukemia. Blood 2013, 122(6):1017-1025. 10.1182/blood-2013-04-497644.
44. Davies M.N., Volta M., Pidsley R., Lunnon K., Dixit A., Lovestone S., et al. Functional annotation of the human brain methylome identifies tissue-specific epigenetic variation across brain and blood. Genome Biology 2012, R43. 10.1186/gb-2012-13-6-r43.
45. Della Ragione F., Criniti V., Della Pietra V., Borriello A., Oliva A., Indaco S., et al. Genes modulated by histone acetylation as new effectors of butyrate activity. FEBS Letters 2001, 499(3):199-204.
46. Dempster E.L., Mill J., Craig I.W., Collier D.A. The quantification of COMT mRNA in post mortem cerebellum tissue: Diagnosis, genotype, methylation and expression. BMC Medical Genetics 2006, 7:10. 10.1186/1471-2350-7-10.
47. Dempster E.L., Pidsley R., Schalkwyk L.C., Owens S., Georgiades A., Kane F., et al. Disease-associated epigenetic changes in monozygotic twins discordant for schizophrenia and bipolar disorder. Human Molecular Genetics 2011, 20(24):4786-4796. 10.1093/hmg/ddr416.
48. Desaulniers D., Xiao G.H., Leingartner K., Chu I., Musicki B., Tsang B.K. Comparisons of brain, uterus, and liver mRNA expression for cytochrome p450s, DNA methyltransferase-1, and catechol-o-methyltransferase in prepubertal female Sprague-Dawley rats exposed to a mixture of aryl hydrocarbon receptor agonists. Toxicological Sciences: An Official Journal of the Society of Toxicology 2005, 86(1):175-184. 10.1093/toxsci/kfi178.
49. Dias B.G., Ressler K.J. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nature Neuroscience 2014, 17(1):89-96. 10.1038/nn.3594.
50. Dong E., Gavin D.P., Chen Y., Davis J. Upregulation of TET1 and downregulation of APOBEC3A and APOBEC3C in the parietal cortex of psychotic patients. Translational Psychiatry 2012, 2:e159. 10.1038/tp.2012.86.
51. Dong E., Nelson M., Grayson D.R., Costa E., Guidotti A. Clozapine and sulpiride but not haloperidol or olanzapine activate brain DNA demethylation. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(36):13614-13619. 10.1073/pnas.0805493105.
52. Drobic B., Perez-Cadahia B., Yu J., Kung S.K., Davie J.R. Promoter chromatin remodeling of immediate-early genes is mediated through H3 phosphorylation at either serine 28 or 10 by the MSK1 multi-protein complex. Nucleic Acids Research 2010, 38(10):3196-3208. 10.1093/nar/gkq030.
53. Endres M., Meisel A., Biniszkiewicz D., Namura S., Prass K., Ruscher K., et al. DNA methyltransferase contributes to delayed ischemic brain injury. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2000, 20(9):3175-3181.
54. Epsztejn-Litman S., Feldman N., Abu-Remaileh M., Shufaro Y., Gerson A., Ueda J., et al. De novo DNA methylation promoted by G9a prevents reprogramming of embryonically silenced genes. Nature Structural & Molecular Biology 2008, 15(11):1176-1183. 10.1038/nsmb.1476.
55. Esteve P.O., Chin H.G., Smallwood A., Feehery G.R., Gangisetty O., Karpf A.R., et al. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes & Development 2006, 20(22):3089-3103. 10.1101/gad.1463706.
56. Fessler E.B., Chibane F.L., Wang Z., Chuang D.M. Potential roles of HDAC inhibitors in mitigating ischemia-induced brain damage and facilitating endogenous regeneration and recovery. Current Pharmaceutical Design 2013, 19(28):5105-5120.
57. Fischer A., Sananbenesi F., Mungenast A., Tsai L.H. Targeting the correct HDAC(s) to treat cognitive disorders. Trends in Pharmacological Sciences 2010, 31(12):605-617. 10.1016/j.tips.2010.09.003.
58. Fujita Y., Morinobu S., Takei S., Fuchikami M., Matsumoto T., Yamamoto S., et al. Vorinostat, a histone deacetylase inhibitor, facilitates fear extinction and enhances expression of the hippocampal NR2B-containing NMDA receptor gene. Journal of Psychiatric Research 2012, 46(5):635-643. 10.1016/j.jpsychires.2012.01.026.
59. Fuks F., Burgers W.A., Brehm A., Hughes-Davies L., Kouzarides T. DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nature Genetics 2000, 24(1):88-91. 10.1038/71750.
60. Fuks F., Burgers W.A., Godin N., Kasai M., Kouzarides T. Dnmt3a binds deacetylases and is recruited by a sequence-specific repressor to silence transcription. The EMBO Journal 2001, 20(10):2536-2544. 10.1093/emboj/20.10.2536.
61. Fuks F., Hurd P.J., Deplus R., Kouzarides T. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Research 2003, 31(9):2305-2312.
62. Fuks F., Hurd P.J., Wolf D., Nan X., Bird A.P., Kouzarides T. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. The Journal of Biological Chemistry 2003, 278(6):4035-4040. 10.1074/jbc.M210256200.
63. Gavin D.P., Akbarian S. Epigenetic and post-transcriptional dysregulation of gene expression in schizophrenia and related disease. Neurobiology of Disease 2012, 46(2):255-262. 10.1016/j.nbd.2011.12.008.
64. Gavin D.P., Chase K.A., Sharma R.P. Active DNA demethylation in post-mitotic neurons: A reason for optimism. Neuropharmacology 2013, 75:233-245. 10.1016/j.neuropharm.2013.07.036.
65. Gavin D.P., Kartan S., Chase K., Grayson D.R., Sharma R.P. Reduced baseline acetylated histone 3 levels, and a blunted response to HDAC inhibition in lymphocyte cultures from schizophrenia subjects. Schizophrenia Research 2008, 103(1-3):330-332. 10.1016/j.schres.2008.04.026.
66. Gavin D.P., Kartan S., Chase K., Jayaraman S., Sharma R.P. Histone deacetylase inhibitors and candidate gene expression: An in vivo and in vitro approach to studying chromatin remodeling in a clinical population. Journal of Psychiatric Research 2009, 43(9):870-876. 10.1016/j.jpsychires.2008.12.006.
67. Gavin D.P., Rosen C., Chase K., Grayson D.R., Tun N., Sharma R.P. Dimethylated lysine 9 of histone 3 is elevated in schizophrenia and exhibits a divergent response to histone deacetylase inhibitors in lymphocyte cultures. Journal of Psychiatry & Neuroscience: JPN 2009, 34(3):232-237.
68. Gavin D.P., Sharma R.P., Chase K.A., Matrisciano F., Dong E., Guidotti A. Growth arrest and DNA-damage-inducible, beta (GADD45b)-mediated DNA demethylation in major psychosis. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 2012, 37(2):531-542. 10.1038/npp.2011.221.
69. Gehring M., Bubb K.L., Henikoff S. Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science (New York, NY) 2009, 324(5933):1447-1451. 10.1126/science.1171609.
70. Ghadirivasfi M., Nohesara S., Ahmadkhaniha H.R., Eskandari M.R., Mostafavi S., Thiagalingam S., et al. Hypomethylation of the serotonin receptor type-2A gene (HTR2A) at T102C polymorphic site in DNA derived from the saliva of patients with schizophrenia and bipolar disorder. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics: The Official Publication of the International Society of Psychiatric Genetics 2011, 156B(5):536-545. 10.1002/ajmg.b.31192.
71. Glatt S.J., Stone W.S., Nossova N., Liew C.C., Seidman L.J., Tsuang M.T. Similarities and differences in peripheral blood gene-expression signatures of individuals with schizophrenia and their first-degree biological relatives. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics: The Official Publication of the International Society of Psychiatric Genetics 2011, 156B(8):869-887. 10.1002/ajmg.b.31239.
72. Goldberg S., Visochek L., Giladi E., Gozes I., Cohen-Armon M. PolyADP-ribosylation is required for long-term memory formation in mammals. Journal of Neurochemistry 2009, 111(1):72-79. 10.1111/j.1471-4159.2009.06296.x.
73. Gottlicher M., Minucci S., Zhu P., Kramer O.H., Schimpf A., Giavara S., et al. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. The EMBO Journal 2001, 20(24):6969-6978. 10.1093/emboj/20.24.6969.
74. Grayson D.R., Jia X., Chen Y., Sharma R.P., Mitchell C.P., Guidotti A., et al. Reelin promoter hypermethylation in schizophrenia. Proceedings of the National Academy of Sciences of the United States of America 2005, 102(26):9341-9346. 10.1073/pnas.0503736102.
75. Grayson D.R., Kundakovic M., Sharma R.P. Is there a future for histone deacetylase inhibitors in the pharmacotherapy of psychiatric disorders?. Molecular Pharmacology 2010, 77(2):126-135. 10.1124/mol.109.061333.
76. Guidotti A., Auta J., Chen Y., Davis J.M., Dong E., Gavin D.P., et al. Epigenetic GABAergic targets in schizophrenia and bipolar disorder. Neuropharmacology 2011, 60(7-8):1007-1016. 10.1016/j.neuropharm.2010.10.021.
77. Guidotti A., Ruzicka W., Grayson D.R., Veldic M., Pinna G., Davis J.M., et al. S-adenosyl methionine and DNA methyltransferase-1 mRNA overexpression in psychosis. Neuroreport 2007, 18(1):57-60. 10.1097/WNR.0b013e32800fefd7.
78. Guo J.U., Ma D.K., Mo H., Ball M.P., Jang M.H., Bonaguidi M.A., et al. Neuronal activity modifies the DNA methylation landscape in the adult brain. Nature Neuroscience 2011, 14(10):1345-1351. 10.1038/nn.2900.
79. Guo J.U., Su Y., Zhong C., Ming G.L., Song H. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 2011, 145(3):423-434. 10.1016/j.cell.2011.03.022.
80. Hahn M.A., Qiu R., Wu X., Li A.X., Zhang H., Wang J., et al. Dynamics of 5-hydroxymethylcytosine and chromatin marks in mammalian neurogenesis. Cell Reports 2013, 3(2):291. 10.1016/j.celrep.2013.01.011.
81. Hassa P.O., Haenni S.S., Buerki C., Meier N.I., Lane W.S., Owen H., et al. Acetylation of poly(ADP-ribose) polymerase-1 by p300/CREB-binding protein regulates coactivation of NF-kappaB-dependent transcription. The Journal of Biological Chemistry 2005, 280(49):40450-40464. 10.1074/jbc.M507553200.
82. He Y.F., Li B.Z., Li Z., Liu P., Wang Y., Tang Q., et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science (New York, NY) 2011, 333(6047):1303-1307. 10.1126/science.1210944.
83. Hendrich B., Hardeland U., Ng H.H., Jiricny J., Bird A. The thymine glycosylase MBD4 can bind to the product of deamination at methylated CpG sites. Nature 1999, 401(6750):301-304. 10.1038/45843.
84. Hernandez A.I., Wolk J., Hu J.Y., Liu J., Kurosu T., Schwartz J.H., et al. Poly-(ADP-ribose) polymerase-1 is necessary for long-term facilitation in aplysia. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 2009, 29(30):9553-9562. 10.1523/JNEUROSCI.1512-09.2009.
85. Herz H.M., Garruss A., Shilatifard A. SET for life: Biochemical activities and biological functions of SET domain-containing proteins. Trends in Biochemical Sciences 2013, 38(12):621-639. 10.1016/j.tibs.2013.09.004.
86. Hevroni D., Rattner A., Bundman M., Lederfein D., Gabarah A., Mangelus M., et al. Hippocampal plasticity involves extensive gene induction and multiple cellular mechanisms. Journal of Molecular Neuroscience: MN 1998, 10(2):75-98. 10.1007/BF02737120.
87. Hirose T., Sowa Y., Takahashi S., Saito S., Yasuda C., Shindo N., et al. p53-independent induction of Gadd45 by histone deacetylase inhibitor: Coordinate regulation by transcription factors oct-1 and NF-Y. Oncogene 2003, 22(49):7762-7773. 10.1038/sj.onc.1207091.
88. Hirota T., Lipp J.J., Toh B.H., Peters J.M. Histone H3 serine 10 phosphorylation by aurora B causes HP1 dissociation from heterochromatin. Nature 2005, 438(7071):1176-1180. 10.1038/nature04254.
89. Hong L., Schroth G.P., Matthews H.R., Yau P., Bradbury E.M. Studies of the DNA binding properties of histone H4 amino terminus. Thermal denaturation studies reveal that acetylation markedly reduces the binding constant of the H4 "tail" to DNA. The Journal of Biological Chemistry 1993, 268(1):305-314.
90. Huang H.S., Akbarian S. GAD1 mRNA expression and DNA methylation in prefrontal cortex of subjects with schizophrenia. PLoS One 2007, 2(8):e809. 10.1371/journal.pone.0000809.
91. Huang H.S., Matevossian A., Whittle C., Kim S.Y., Schumacher A., Baker S.P., et al. Prefrontal dysfunction in schizophrenia involves mixed-lineage leukemia 1-regulated histone methylation at GABAergic gene promoters. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2007, 27(42):11254-11262. 10.1523/JNEUROSCI.3272-07.2007.
92. Huang W., Mishra V., Batra S., Dillon I., Mehta K.D. Phorbol ester promotes histone H3-Ser10 phosphorylation at the LDL receptor promoter in a protein kinase C-dependent manner. Journal of Lipid Research 2004, 45(8):1519-1527. 10.1194/jlr.M400088-JLR200.
93. Ikegame T., Bundo M., Sunaga F., Asai T., Nishimura F., Yoshikawa A., et al. DNA methylation analysis of BDNF gene promoters in peripheral blood cells of schizophrenia patients. Neuroscience Research 2013, 77(4):208-214. 10.1016/j.neures.2013.08.004.
94. Issidorides M.R., Stefanis C.N., Varsou E., Katsorchis T. Altered chromatin ultrastructure in neutrophils of schizophrenics. Nature 1975, 258(5536):612-614.
95. Ito S., D'Alessio A.C., Taranova O.V., Hong K., Sowers L.C., Zhang Y. Role of tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 2010, 466(7310):1129-1133. 10.1038/nature09303.
96. Ito S., Shen L., Dai Q., Wu S.C., Collins L.B., Swenberg J.A., et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science (New York, NY) 2011, 333(6047):1300-1303. 10.1126/science.1210597.
97. Itzhak Y., Liddie S., Anderson K.L. Sodium butyrate-induced histone acetylation strengthens the expression of cocaine-associated contextual memory. Neurobiology of Learning and Memory 2013, 102:34-42. 10.1016/j.nlm.2013.03.007.
98. Iwamoto K., Bundo M., Yamada K., Takao H., Iwayama-Shigeno Y., Yoshikawa T., et al. DNA methylation status of SOX10 correlates with its downregulation and oligodendrocyte dysfunction in schizophrenia. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2005, 25(22):5376-5381. 10.1523/JNEUROSCI.0766-05.2005.
99. Jakovcevski M., Bharadwaj R., Straubhaar J., Gao G., Gavin D.P., Jakovcevski I., et al. Prefrontal cortical dysfunction after overexpression of histone deacetylase 1. Biological Psychiatry 2013, 74(9):696-705. 10.1016/j.biopsych.2013.03.020.
100. Jiang Y., Jakovcevski M., Bharadwaj R., Connor C., Schroeder F.A., Lin C.L., et al. Setdb1 histone methyltransferase regulates mood-related behaviors and expression of the NMDA receptor subunit NR2B. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2010, 30(21):7152-7167. 10.1523/JNEUROSCI.1314-10.2010.
101. Jiang Y., Langley B., Lubin F.D., Renthal W., Wood M.A., Yasui D.H., et al. Epigenetics in the nervous system. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2008, 28(46):11753-11759. 10.1523/jneurosci.3797-08.2008.
102. Jorgensen T.J., Chen K., Chasovskikh S., Roy R., Dritschilo A., Uren A. Binding kinetics and activity of human poly(ADP-ribose) polymerase-1 on oligo-deoxyribonucleotide substrates. Journal of Molecular Recognition: JMR 2009, 22(6):446-452. 10.1002/jmr.962.
103. Kaas G.A., Zhong C., Eason D.E., Ross D.L., Vachhani R.V., Ming G.L., et al. TET1 controls CNS 5-methylcytosine hydroxylation, active DNA demethylation, gene transcription, and memory formation. Neuron 2013, 79(6):1086-1093. 10.1016/j.neuron.2013.08.032.
104. Kangaspeska S., Stride B., Metivier R., Polycarpou-Schwarz M., Ibberson D., Carmouche R.P., et al. Transient cyclical methylation of promoter DNA. Nature 2008, 452(7183):112-115. 10.1038/nature06640.
105. Keeley M.B., Wood M.A., Isiegas C., Stein J., Hellman K., Hannenhalli S., et al. Differential transcriptional response to nonassociative and associative components of classical fear conditioning in the amygdala and hippocampus. Learning & Memory (Cold Spring Harbor, NY) 2006, 13(2):135-142. 10.1101/lm.86906.
106. Kemmerich K., Dingler F.A., Rada C., Neuberger M.S. Germline ablation of SMUG1 DNA glycosylase causes loss of 5-hydroxymethyluracil- and UNG-backup uracil-excision activities and increases cancer predisposition of ung-/-Msh2-/- mice. Nucleic Acids Research 2012, 40(13):6016-6025. 10.1093/nar/gks259.
107. Kennedy P.J., Feng J., Robison A.J., Maze I., Badimon A., Mouzon E., et al. Class I HDAC inhibition blocks cocaine-induced plasticity by targeted changes in histone methylation. Nature Neuroscience 2013, 16(4):434-440. 10.1038/nn.3354.
108. Kim Y.I. Methylenetetrahydrofolate reductase polymorphisms, folate, and cancer risk: A paradigm of gene-nutrient interactions in carcinogenesis. Nutrition Reviews 2000, 58(7):205-209.
109. Kim G.D., Ni J., Kelesoglu N., Roberts R.J., Pradhan S. Co-operation and communication between the human maintenance and de novo DNA (cytosine-5) methyltransferases. The EMBO Journal 2002, 21(15):4183-4195.
110. Kim H.J., Rowe M., Ren M., Hong J.S., Chen P.S., Chuang D.M. Histone deacetylase inhibitors exhibit anti-inflammatory and neuroprotective effects in a rat permanent ischemic model of stroke: Multiple mechanisms of action. The Journal of Pharmacology and Experimental Therapeutics 2007, 321(3):892-901. 10.1124/jpet.107.120188.
111. Kinoshita M., Numata S., Tajima A., Shimodera S., Imoto I., Ohmori T. Plasma total homocysteine is associated with DNA methylation in patients with schizophrenia. Epigenetics: Official Journal of the DNA Methylation Society 2013, 8(6):584-590. 10.4161/epi.24621.
112. Kloukina-Pantazidou I., Havaki S., Chrysanthou-Piterou M., Kontaxakis V.P., Papadimitriou G.N., Issidorides M.R. Chromatin alterations in leukocytes of first-episode schizophrenic patients. Ultrastructural Pathology 2010, 34(3):106-116. 10.3109/01913121003644781.
113. Kordi-Tamandani D.M., Dahmardeh N., Torkamanzehi A. Evaluation of hypermethylation and expression pattern of GMR2, GMR5, GMR8, and GRIA3 in patients with schizophrenia. Gene 2013, 515(1):163-166. 10.1016/j.gene.2012.10.075.
114. Koseki T., Mouri A., Mamiya T., Aoyama Y., Toriumi K., Suzuki S., et al. Exposure to enriched environments during adolescence prevents abnormal behaviours associated with histone deacetylation in phencyclidine-treated mice. The International Journal of Neuropsychopharmacology/Official Scientific Journal of the Collegium Internationale Neuropsychopharmacologicum (CINP) 2012, 15(10):1489-1501. 10.1017/S1461145711001672.
115. Kozlenkov A., Roussos P., Timashpolsky A., Barbu M., Rudchenko S., Bibikova M., et al. Differences in DNA methylation between human neuronal and glial cells are concentrated in enhancers and non-CpG sites. Nucleic Acids Research 2014, 42(1):109-127. 10.1093/nar/gkt838.
116. Kress C., Thomassin H., Grange T. Local DNA demethylation in vertebrates: How could it be performed and targeted?. FEBS Letters 2001, 494(3):135-140.
117. Kumar A., Choi K.H., Renthal W., Tsankova N.M., Theobald D.E., Truong H.T., et al. Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 2005, 48(2):303-314. 10.1016/j.neuron.2005.09.023.
118. Kuratomi G., Iwamoto K., Bundo M., Kusumi I., Kato N., Iwata N., et al. Aberrant DNA methylation associated with bipolar disorder identified from discordant monozygotic twins. Molecular Psychiatry 2008, 13(4):429-441. 10.1038/sj.mp.4002001.
119. Kurian J.R., Keen K.L., Terasawa E. Epigenetic changes coincide with in vitro primate GnRH neuronal maturation. Endocrinology 2010, 151(11):5359-5368. 10.1210/en.2010-0555.
120. Kurita M., Holloway T., Garcia-Bea A., Kozlenkov A., Friedman A.K., Moreno J.L., et al. HDAC2 regulates atypical antipsychotic responses through the modulation of mGlu2 promoter activity. Nature Neuroscience 2012, 15(9):1245-1254. 10.1038/nn.3181.
121. Labrie V., Pai S., Petronis A. Epigenetics of major psychosis: Progress, problems and perspectives. Trends in Genetics: TIG 2012, 28(9):427-435. 10.1016/j.tig.2012.04.002.
122. Langelier M.F., Planck J.L., Roy S., Pascal J.M. Structural basis for DNA damage-dependent poly(ADP-ribosyl)ation by human PARP-1. Science (New York, NY) 2012, 336(6082):728-732. 10.1126/science.1216338.
123. Laurent L., Wong E., Li G., Huynh T., Tsirigos A., Ong C.T., et al. Dynamic changes in the human methylome during differentiation. Genome Research 2010, 20(3):320-331. 10.1101/gr.101907.109.
124. Leach P.T., Poplawski S.G., Kenney J.W., Hoffman B., Liebermann D.A., Abel T., et al. Gadd45b knockout mice exhibit selective deficits in hippocampus-dependent long-term memory. Learning & Memory (Cold Spring Harbor, NY) 2012, 19(8):319-324. 10.1101/lm.024984.111.
125. Lee W.J., Shim J.Y., Zhu B.T. Mechanisms for the inhibition of DNA methyltransferases by tea catechins and bioflavonoids. Molecular Pharmacology 2005, 68(4):1018-1030. 10.1124/mol.104.008367.
126. Lee M.G., Wynder C., Schmidt D.M., McCafferty D.G., Shiekhattar R. Histone H3 lysine 4 demethylation is a target of nonselective antidepressive medications. Chemistry & Biology 2006, 13(6):563-567. 10.1016/j.chembiol.2006.05.004.
127. Lee B.H., Yegnasubramanian S., Lin X., Nelson W.G. Procainamide is a specific inhibitor of DNA methyltransferase 1. The Journal of Biological Chemistry 2005, 280(49):40749-40756. 10.1074/jbc.M505593200.
128. Lemberger T., Parkitna J.R., Chai M., Schutz G., Engblom D. CREB has a context-dependent role in activity-regulated transcription and maintains neuronal cholesterol homeostasis. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 2008, 22(8):2872-2879. 10.1096/fj.08-107888.
129. Li J., Guo Y., Schroeder F.A., Youngs R.M., Schmidt T.W., Ferris C., et al. Dopamine D2-like antagonists induce chromatin remodeling in striatal neurons through cyclic AMP-protein kinase A and NMDA receptor signaling. Journal of Neurochemistry 2004, 90(5):1117-1131. 10.1111/j.1471-4159.2004.02569.x.
130. Lim S., Metzger E., Schule R., Kirfel J., Buettner R. Epigenetic regulation of cancer growth by histone demethylases. International Journal of Cancer. Journal International Du Cancer 2010, 127(9):1991-1998. 10.1002/ijc.25538.
131. Lister R., Mukamel E.A., Nery J.R., Urich M., Puddifoot C.A., Johnson N.D., et al. Global epigenomic reconfiguration during mammalian brain development. Science (New York, NY) 2013, 341(6146):1237905. 10.1126/science.1237905.
132. Lister R., Pelizzola M., Dowen R.H., Hawkins R.D., Hon G., Tonti-Filippini J., et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009, 462(7271):315-322. 10.1038/nature08514.
133. Lomniczi A., Loche A., Castellano J.M., Ronnekleiv O.K., Bosch M., Kaidar G., et al. Epigenetic control of female puberty. Nature Neuroscience 2013, 16(3):281-289. 10.1038/nn.3319.
134. Ma D.K., Jang M.H., Guo J.U., Kitabatake Y., Chang M.L., Pow-Anpongkul N., et al. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science (New York, NY) 2009, 323(5917):1074-1077. 10.1126/science.1166859.
135. Mackowiak M., Guzik R., Dudys D., Bator E., Wedzony K. MK-801, a NMDA receptor antagonist, increases phosphorylation of histone H3 in the rat medial prefrontal cortex. Pharmacological Reports: PR 2013, 65(5):1112-1123.
136. Maiti A., Drohat A.C. Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: Potential implications for active demethylation of CpG sites. The Journal of Biological Chemistry 2011, 286(41):35334-35338. 10.1074/jbc.C111.284620.
137. Malvaez M., McQuown S.C., Rogge G.A., Astarabadi M., Jacques V., Carreiro S., et al. HDAC3-selective inhibitor enhances extinction of cocaine-seeking behavior in a persistent manner. Proceedings of the National Academy of Sciences of the United States of America 2013, 110(7):2647-2652. 10.1073/pnas.1213364110.
138. Martinowich K., Hattori D., Wu H., Fouse S., He F., Hu Y., et al. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science (New York, NY) 2003, 302(5646):890-893. 10.1126/science.1090842.
139. Marutha Ravindran C.R., Ticku M.K. Role of CpG islands in the up-regulation of NMDA receptor NR2B gene expression following chronic ethanol treatment of cultured cortical neurons of mice. Neurochemistry International 2005, 46(4):313-327. 10.1016/j.neuint.2004.10.004.
140. Masson M., Menissier-de Murcia J., Mattei M.G., de Murcia G., Niedergang C.P. Poly(ADP-ribose) polymerase interacts with a novel human ubiquitin conjugating enzyme: HUbc9. Gene 1997, 190(2):287-296.
141. Matsui T., Leung D., Miyashita H., Maksakova I.A., Miyachi H., Kimura H., et al. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 2010, 464(7290):927-931. 10.1038/nature08858.
142. McGowan P.O. Epigenomic mechanisms of early adversity and HPA dysfunction: Considerations for PTSD research. Frontiers in Psychiatry 2013, 4:110. 10.3389/fpsyt.2013.00110.
143. McGowan P.O., Sasaki A., D'Alessio A.C., Dymov S., Labonte B., Szyf M., et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nature Neuroscience 2009, 12(3):342-348. 10.1038/nn.2270.
144. Melas P.A., Rogdaki M., Osby U., Schalling M., Lavebratt C., Ekstrom T.J. Epigenetic aberrations in leukocytes of patients with schizophrenia: Association of global DNA methylation with antipsychotic drug treatment and disease onset. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 2012, 26(6):2712-2718. 10.1096/fj.11-202069.
145. Mendoza-Alvarez H., Alvarez-Gonzalez R. Poly(ADP-ribose) polymerase is a catalytic dimer and the automodification reaction is intermolecular. The Journal of Biological Chemistry 1993, 268(30):22575-22580.
146. Messner S., Altmeyer M., Zhao H., Pozivil A., Roschitzki B., Gehrig P., et al. PARP1 ADP-ribosylates lysine residues of the core histone tails. Nucleic Acids Research 2010, 38(19):6350-6362. 10.1093/nar/gkq463.
147. Messner S., Schuermann D., Altmeyer M., Kassner I., Schmidt D., Schar P., et al. Sumoylation of poly(ADP-ribose) polymerase 1 inhibits its acetylation and restrains transcriptional coactivator function. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 2009, 23(11):3978-3989. 10.1096/fj.09-137695.
148. Metivier R., Gallais R., Tiffoche C., Le Peron C., Jurkowska R.Z., Carmouche R.P., et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008, 452(7183):45-50. 10.1038/nature06544.
149. Metzger E., Wissmann M., Yin N., Muller J.M., Schneider R., Peters A.H., et al. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 2005, 437(7057):436-439. 10.1038/nature04020.
150. Mifsud K.R., Gutierrez-Mecinas M., Trollope A.F., Collins A., Saunderson E.A., Reul J.M. Epigenetic mechanisms in stress and adaptation. Brain, Behavior, and Immunity 2011, 25(7):1305-1315. 10.1016/j.bbi.2011.06.005.
151. Mill J., Tang T., Kaminsky Z., Khare T., Yazdanpanah S., Bouchard L., et al. Epigenomic profiling reveals DNA-methylation changes associated with major psychosis. American Journal of Human Genetics 2008, 82(3):696-711. 10.1016/j.ajhg.2008.01.008.
152. Mimasu S., Umezawa N., Sato S., Higuchi T., Umehara T., Yokoyama S. Structurally designed trans-2-phenylcyclopropylamine derivatives potently inhibit histone demethylase LSD1/KDM1. Biochemistry 2010, 49(30):6494-6503. 10.1021/bi100299r.
153. Morgan H.D., Dean W., Coker H.A., Reik W., Petersen-Mahrt S.K. Activation-induced cytidine deaminase deaminates 5-methylcytosine in DNA and is expressed in pluripotent tissues: Implications for epigenetic reprogramming. The Journal of Biological Chemistry 2004, 279(50):52353-52360. 10.1074/jbc.M407695200.
154. Murphy B.C., O'Reilly R.L., Singh S.M. Site-specific cytosine methylation in S-COMT promoter in 31 brain regions with implications for studies involving schizophrenia. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics: The Official Publication of the International Society of Psychiatric Genetics 2005, 133B(1):37-42. 10.1002/ajmg.b.30134.
155. Nan X., Ng H.H., Johnson C.A., Laherty C.D., Turner B.M., Eisenman R.N., et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998, 393(6683):386-389. 10.1038/30764.
156. Naveh-Many T., Cedar H. Active gene sequences are undermethylated. Proceedings of the National Academy of Sciences of the United States of America 1981, 78(7):4246-4250.
157. Nestler E.J. Epigenetic mechanisms of drug addiction. Neuropharmacology 2014, 76(Pt B):259-268. 10.1016/j.neuropharm.2013.04.004.
158. Nishioka M., Bundo M., Koike S., Takizawa R., Kakiuchi C., Araki T., et al. Comprehensive DNA methylation analysis of peripheral blood cells derived from patients with first-episode schizophrenia. Journal of Human Genetics 2013, 58(2):91-97. 10.1038/jhg.2012.140.
159. Nohesara S., Ghadirivasfi M., Mostafavi S., Eskandari M.R., Ahmadkhaniha H., Thiagalingam S., et al. DNA hypomethylation of MB-COMT promoter in the DNA derived from saliva in schizophrenia and bipolar disorder. Journal of Psychiatric Research 2011, 45(11):1432-1438. 10.1016/j.jpsychires.2011.06.013.
160. Numachi Y., Shen H., Yoshida S., Fujiyama K., Toda S., Matsuoka H., et al. Methamphetamine alters expression of DNA methyltransferase 1 mRNA in rat brain. Neuroscience Letters 2007, 414(3):213-217. 10.1016/j.neulet.2006.12.052.
161. Numachi Y., Yoshida S., Yamashita M., Fujiyama K., Naka M., Matsuoka H., et al. Psychostimulant alters expression of DNA methyltransferase mRNA in the rat brain. Annals of the New York Academy of Sciences 2004, 1025:102-109. 10.1196/annals.1316.013.
162. Ooi S.K., Bestor T.H. The colorful history of active DNA demethylation. Cell 2008, 133(7):1145-1148. 10.1016/j.cell.2008.06.009.
163. Ooi S.K., Qiu C., Bernstein E., Li K., Jia D., Yang Z., et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 2007, 448(7154):714-717. 10.1038/nature05987.
164. Pastor W.A., Pape U.J., Huang Y., Henderson H.R., Lister R., Ko M., et al. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 2011, 473(7347):394-397. 10.1038/nature10102.
165. Patil S.T., Zhang L., Martenyi F., Lowe S.L., Jackson K.A., Andreev B.V., et al. Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: A randomized phase 2 clinical trial. Nature Medicine 2007, 13(9):1102-1107. 10.1038/nm1632.
166. Petronis A., Gottesman I.I., Kan P., Kennedy J.L., Basile V.S., Paterson A.D., et al. Monozygotic twins exhibit numerous epigenetic differences: Clues to twin discordance?. Schizophrenia Bulletin 2003, 29(1):169-178.
167. Phiel C.J., Zhang F., Huang E.Y., Guenther M.G., Lazar M.A., Klein P.S. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. The Journal of Biological Chemistry 2001, 276(39):36734-36741. 10.1074/jbc.M101287200.
168. Popp C., Dean W., Feng S., Cokus S.J., Andrews S., Pellegrini M., et al. Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 2010, 463(7284):1101-1105. 10.1038/nature08829.
169. Rai K., Huggins I.J., James S.R., Karpf A.R., Jones D.A., Cairns B.R. DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 2008, 135(7):1201-1212. 10.1016/j.cell.2008.11.042.
170. Ramanathan B., Smerdon M.J. Enhanced DNA repair synthesis in hyperacetylated nucleosomes. The Journal of Biological Chemistry 1989, 264(19):11026-11034.
171. Rampon C., Jiang C.H., Dong H., Tang Y.P., Lockhart D.J., Schultz P.G., et al. Effects of environmental enrichment on gene expression in the brain. Proceedings of the National Academy of Sciences of the United States of America 2000, 97(23):12880-12884. 10.1073/pnas.97.23.12880.
172. Rauch T.A., Wu X., Zhong X., Riggs A.D., Pfeifer G.P. A human B cell methylome at 100-base pair resolution. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(3):671-678. 10.1073/pnas.0812399106.
173. Raybuck J.D., McCleery E.J., Cunningham C.L., Wood M.A., Lattal K.M. The histone deacetylase inhibitor sodium butyrate modulates acquisition and extinction of cocaine-induced conditioned place preference. Pharmacology, Biochemistry, and Behavior 2013, 106:109-116. 10.1016/j.pbb.2013.02.009.
174. Razin A., Riggs A.D. DNA methylation and gene function. Science (New York, NY) 1980, 210(4470):604-610.
175. Rice D.S., Curran T. Role of the reelin signaling pathway in central nervous system development. Annual Review of Neuroscience 2001, 24:1005-1039. 10.1146/annurev.neuro.24.1.1005.
176. Ricobaraza A., Cuadrado-Tejedor M., Marco S., Perez-Otano I., Garcia-Osta A. Phenylbutyrate rescues dendritic spine loss associated with memory deficits in a mouse model of Alzheimer disease. Hippocampus 2012, 22(5):1040-1050. 10.1002/hipo.20883.
177. Robertson K.D., Ait-Si-Ali S., Yokochi T., Wade P.A., Jones P.L., Wolffe A.P. DNMT1 forms a complex with rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nature Genetics 2000, 25(3):338-342. 10.1038/77124.
178. Robertson J., Robertson A.B., Klungland A. The presence of 5-hydroxymethylcytosine at the gene promoter and not in the gene body negatively regulates gene expression. Biochemical and Biophysical Research Communications 2011, 411(1):40-43. 10.1016/j.bbrc.2011.06.077.
179. Roemer I., Reik W., Dean W., Klose J. Epigenetic inheritance in the mouse. Current Biology: CB 1997, 7(4):277-280.
180. Rotili D., Tomassi S., Conte M., Benedetti R., Tortorici M., Ciossani G., et al. Pan-histone demethylase inhibitors simultaneously targeting jumonji C and lysine-specific demethylases display high anticancer activities. Journal of Medicinal Chemistry 2014, 57(1):42-55. 10.1021/jm4012802.
181. Rotllant D., Armario A. Brain pattern of histone H3 phosphorylation after acute amphetamine administration: Its relationship to brain c-fos induction is strongly dependent on the particular brain area. Neuropharmacology 2012, 62(2):1073-1081. 10.1016/j.neuropharm.2011.10.019.
182. Rountree M.R., Bachman K.E., Baylin S.B. DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nature Genetics 2000, 25(3):269-277. 10.1038/77023.
183. Rudenko A., Dawlaty M.M., Seo J., Cheng A.W., Meng J., Le T., et al. Tet1 is critical for neuronal activity-regulated gene expression and memory extinction. Neuron 2013, 79(6):1109-1122. 10.1016/j.neuron.2013.08.003.
184. Russo V.E.A., Martienssen R.A., Riggs A.D. Epigenetic mechanisms of gene regulation 1996, Cold Spring Harbor Laboratory Press, Plainview, NY.
185. Ruzicka W.B., Zhubi A., Veldic M., Grayson D.R., Costa E., Guidotti A. Selective epigenetic alteration of layer I GABAergic neurons isolated from prefrontal cortex of schizophrenia patients using laser-assisted microdissection. Molecular Psychiatry 2007, 12(4):385-397. 10.1038/sj.mp.4001954.
186. Ryu H., Al-Ani G., Deckert K., Kirkpatrick D., Gygi S.P., Dasso M., et al. PIASy mediates SUMO-2/3 conjugation of poly(ADP-ribose) polymerase 1 (PARP1) on mitotic chromosomes. The Journal of Biological Chemistry 2010, 285(19):14415-14423. 10.1074/jbc.M109.074583.
187. Ryu H., Lee J., Hagerty S.W., Soh B.Y., McAlpin S.E., Cormier K.A., et al. ESET/SETDB1 gene expression and histone H3 (K9) trimethylation in Huntington's disease. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(50):19176-19181. 10.1073/pnas.0606373103.
188. Sakharkar A.J., Zhang H., Tang L., Shi G., Pandey S.C. Histone deacetylases (HDAC)-induced histone modifications in the amygdala: A role in rapid tolerance to the anxiolytic effects of ethanol. Alcoholism, Clinical and Experimental Research 2012, 36(1):61-71. 10.1111/j.1530-0277.2011.01581.x.
189. Salnikow K., Zhitkovich A. Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis: Nickel, arsenic, and chromium. Chemical Research in Toxicology 2008, 21(1):28-44. 10.1021/tx700198a.
190. San Miguel Amigo L., Franco Osorio R., Mercadal Vilchez S., Martinez-Frances A. Azacitidine adverse effects in patients with myelodysplastic syndromes. Advances in Therapy 2011, 28(Suppl. 4):6-11. 10.1007/s12325-011-0024-2.
191. Satta R., Maloku E., Zhubi A., Pibiri F., Hajos M., Costa E., et al. Nicotine decreases DNA methyltransferase 1 expression and glutamic acid decarboxylase 67 promoter methylation in GABAergic interneurons. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(42):16356-16361. 10.1073/pnas.0808699105.
192. Schroeder M., Hillemacher T., Bleich S., Frieling H. The epigenetic code in depression: Implications for treatment. Clinical Pharmacology and Therapeutics 2012, 91(2):310-314. 10.1038/clpt.2011.282.
193. Schroeder F.A., Lin C.L., Crusio W.E., Akbarian S. Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse. Biological Psychiatry 2007, 62(1):55-64. 10.1016/j.biopsych.2006.06.036.
194. Schwarz C., Volz A., Li C., Leucht S. Valproate for schizophrenia. Cochrane Database of Systematic Reviews (Online) 2008, 3(3):CD004028. 10.1002/14651858.CD004028.pub3.
195. Scobie K.N., Damez-Werno D., Sun H., Shao N., Gancarz A., Panganiban C.H., et al. Essential role of poly(ADP-ribosyl)ation in cocaine action. Proceedings of the National Academy of Sciences of the United States of America 2014, 111(5):2005-2010. 10.1073/pnas.1319703111.
196. Sharma R.P. Schizophrenia, epigenetics and ligand-activated nuclear receptors: A framework for chromatin therapeutics. Schizophrenia Research 2005, 72(2-3):79-90. 10.1016/j.schres.2004.03.001.
197. Sharma R.P. Blood chromatin as a biosensor of the epigenetic milieu: A tool for studies in living psychiatric patients. Epigenomics 2012, 4(5):551-559. 10.2217/epi.12.46.
198. Sharma R.P., Chase K.A. Increasing neuronal 'stemness': Chromatin relaxation and the expression of reprogramming genes in post-mitotic neurons. Medical Hypotheses 2012, 78(4):553-554. 10.1016/j.mehy.2011.12.018.
199. Sharma R.P., Gavin D.P., Chase K.A. Heterochromatin as an incubator for pathology and treatment non-response: Implication for neuropsychiatric illness. The Pharmacogenomics Journal 2012, 12(5):361-367. 10.1038/tpj.2011.64.
200. Sharma R.P., Grayson D.R., Gavin D.P. Histone deactylase 1 expression is increased in the prefrontal cortex of schizophrenia subjects: Analysis of the national brain databank microarray collection. Schizophrenia Research 2008, 98(1-3):111-117. 10.1016/j.schres.2007.09.020.
201. Sharma R.P., Rosen C., Kartan S., Guidotti A., Costa E., Grayson D.R., et al. Valproic acid and chromatin remodeling in schizophrenia and bipolar disorder: Preliminary results from a clinical population. Schizophrenia Research 2006, 88(1-3):227-231. 10.1016/j.schres.2006.07.015.
202. Shen H.Y., Kalda A., Yu L., Ferrara J., Zhu J., Chen J.F. Additive effects of histone deacetylase inhibitors and amphetamine on histone H4 acetylation, cAMP responsive element binding protein phosphorylation and DeltaFosB expression in the striatum and locomotor sensitization in mice. Neuroscience 2008, 157(3):644-655. 10.1016/j.neuroscience.2008.09.019.
203. Shimabukuro M., Jinno Y., Fuke C., Okazaki Y. Haloperidol treatment induces tissue- and sex-specific changes in DNA methylation: A control study using rats. Behavioral and Brain Functions: BBF 2006, 2:37. 10.1186/1744-9081-2-37.
204. Shimabukuro M., Sasaki T., Imamura A., Tsujita T., Fuke C., Umekage T., et al. Global hypomethylation of peripheral leukocyte DNA in male patients with schizophrenia: A potential link between epigenetics and schizophrenia. Journal of Psychiatric Research 2007, 41(12):1042-1046. 10.1016/j.jpsychires.2006.08.006.
205. Shinkai Y., Tachibana M. H3K9 methyltransferase G9a and the related molecule GLP. Genes & Development 2011, 25(8):781-788. 10.1101/gad.2027411.
206. Siegmund K.D., Connor C.M., Campan M., Long T.I., Weisenberger D.J., Biniszkiewicz D., et al. DNA methylation in the human cerebral cortex is dynamically regulated throughout the life span and involves differentiated neurons. PLoS One 2007, 2(9):e895. 10.1371/journal.pone.0000895.
207. Singal R., Ginder G.D. DNA methylation. Blood 1999, 93(12):4059-4070.
208. Spruijt C.G., Gnerlich F., Smits A.H., Pfaffeneder T., Jansen P.W., Bauer C., et al. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 2013, 152(5):1146-1159. 10.1016/j.cell.2013.02.004.
209. Stafford J.M., Raybuck J.D., Ryabinin A.E., Lattal K.M. Increasing histone acetylation in the hippocampus-infralimbic network enhances fear extinction. Biological Psychiatry 2012, 72(1):25-33. 10.1016/j.biopsych.2011.12.012.
210. Stefanis C.N., Issidorides M.R. Histochemical changes in the blood cells of schizophrenic patients under pimozide treatment. Biological Psychiatry 1976, 11(1):53-68.
211. Stimson L., La Thangue N.B. Biomarkers for predicting clinical responses to HDAC inhibitors. Cancer Letters 2009, 280(2):177-183. 10.1016/j.canlet.2009.03.016.
212. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature 2000, 403(6765):41-45. 10.1038/47412.
213. Strosznajder R.P., Czubowicz K., Jesko H., Strosznajder J.B. Poly(ADP-ribose) metabolism in brain and its role in ischemia pathology. Molecular Neurobiology 2010, 41(2-3):187-196. 10.1007/s12035-010-8124-6.
214. Sullivan P.F., Fan C., Perou C.M. Evaluating the comparability of gene expression in blood and brain. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics: The Official Publication of the International Society of Psychiatric Genetics 2006, 141B(3):261-268. 10.1002/ajmg.b.30272.
215. Sultan F.A., Wang J., Tront J., Liebermann D.A., Sweatt J.D. Genetic deletion of gadd45b, a regulator of active DNA demethylation, enhances long-term memory and synaptic plasticity. Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2012, 32:17059-17066.
216. Sun H., Kennedy P.J., Nestler E.J. Epigenetics of the depressed brain: Role of histone acetylation and methylation. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 2013, 38(1):124-137. 10.1038/npp.2012.73.
217. Szulwach K.E., Li X., Li Y., Song C.X., Wu H., Dai Q., et al. 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nature Neuroscience 2011, 14(12):1607-1616. 10.1038/nn.2959.
218. Szyf M. Towards a pharmacology of DNA methylation. Trends in Pharmacological Sciences 2001, 22(7):350-354.
219. Tachibana M., Ueda J., Fukuda M., Takeda N., Ohta T., Iwanari H., et al. Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9. Genes & Development 2005, 19(7):815-826. 10.1101/gad.1284005.
220. Tini M., Benecke A., Um S.J., Torchia J., Evans R.M., Chambon P. Association of CBP/p300 acetylase and thymine DNA glycosylase links DNA repair and transcription. Molecular Cell 2002, 9(2):265-277.
221. Tochigi M., Iwamoto K., Bundo M., Komori A., Sasaki T., Kato N., et al. Methylation status of the reelin promoter region in the brain of schizophrenic patients. Biological Psychiatry 2008, 63(5):530-533. 10.1016/j.biopsych.2007.07.003.
222. Trojer P., Reinberg D. Facultative heterochromatin: Is there a distinctive molecular signature?. Molecular Cell 2007, 28(1):1-13. 10.1016/j.molcel.2007.09.011.
223. Tsankova N.M., Berton O., Renthal W., Kumar A., Neve R.L., Nestler E.J. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nature Neuroscience 2006, 9(4):519-525. 10.1038/nn1659.
224. Tsankova N., Renthal W., Kumar A., Nestler E.J. Epigenetic regulation in psychiatric disorders. Nature Reviews. Neuroscience 2007, 8(5):355-367. 10.1038/nrn2132.
225. Tsujita T., Niikawa N., Yamashita H., Imamura A., Hamada A., Nakane Y., et al. Genomic discordance between monozygotic twins discordant for schizophrenia. The American Journal of Psychiatry 1998, 155(3):422-424.
226. Turner B.M. Cellular memory and the histone code. Cell 2002, 111(3):285-291.
227. Vedadi M., Barsyte-Lovejoy D., Liu F., Rival-Gervier S., Allali-Hassani A., Labrie V., et al. A chemical probe selectively inhibits G9a and GLP methyltransferase activity in cells. Nature Chemical Biology 2011, 7(9):648. 10.1038/nchembio0911-648c.
228. Veldic M., Caruncho H.J., Liu W.S., Davis J., Satta R., Grayson D.R., et al. DNA-methyltransferase 1 mRNA is selectively overexpressed in telencephalic GABAergic interneurons of schizophrenia brains. Proceedings of the National Academy of Sciences of the United States of America 2004, 101(1):348-353. 10.1073/pnas.2637013100.
229. Veldic M., Guidotti A., Maloku E., Davis J.M., Costa E. In psychosis, cortical interneurons overexpress DNA-methyltransferase 1. Proceedings of the National Academy of Sciences of the United States of America 2005, 102(6):2152-2157. 10.1073/pnas.0409665102.
230. Veldic M., Kadriu B., Maloku E., Agis-Balboa R.C., Guidotti A., Davis J.M., et al. Epigenetic mechanisms expressed in basal ganglia GABAergic neurons differentiate schizophrenia from bipolar disorder. Schizophrenia Research 2007, 91(1-3):51-61. 10.1016/j.schres.2006.11.029.
231. Vire E., Brenner C., Deplus R., Blanchon L., Fraga M., Didelot C., et al. The polycomb group protein EZH2 directly controls DNA methylation. Nature 2006, 439(7078):871-874. 10.1038/nature04431.
232. Waddington C.H. An introduction to modern genetics 1939, G. Allen & Unwin Ltd, London.
233. Wang H., An W., Cao R., Xia L., Erdjument-Bromage H., Chatton B., et al. mAM facilitates conversion by ESET of dimethyl to trimethyl lysine 9 of histone H3 to cause transcriptional repression. Molecular Cell 2003, 12(2):475-487.
234. Warnault V., Darcq E., Levine A., Barak S., Ron D. Chromatin remodeling-A novel strategy to control excessive alcohol drinking. Translational Psychiatry 2013, 3:e231. 10.1038/tp.2013.4.
235. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., et al. Epigenetic programming by maternal behavior. Nature Neuroscience 2004, 7(8):847-854. 10.1038/nn1276.
236. Wolff G.L., Kodell R.L., Moore S.R., Cooney C.A. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 1998, 12(11):949-957.
237. Wood J.G., Helfand S.L. Chromatin structure and transposable elements in organismal aging. Frontiers in Genetics 2013, 4:274. 10.3389/fgene.2013.00274.
238. Xu Y., Wu F., Tan L., Kong L., Xiong L., Deng J., et al. Genome-wide regulation of 5hmC, 5mC, and gene expression by Tet1 hydroxylase in mouse embryonic stem cells. Molecular Cell 2011, 42(4):451-464. 10.1016/j.molcel.2011.04.005.
239. Yang S.M., Kim B.J., Norwood Toro L., Skoultchi A.I. H1 linker histone promotes epigenetic silencing by regulating both DNA methylation and histone H3 methylation. Proceedings of the National Academy of Sciences of the United States of America 2013, 110(5):1708-1713. 10.1073/pnas.1213266110.
240. Zee B.M., Levin R.S., Xu B., LeRoy G., Wingreen N.S., Garcia B.A. In vivo residue-specific histone methylation dynamics. The Journal of Biological Chemistry 2010, 285(5):3341-3350. 10.1074/jbc.M109.063784.
241. Zhang R.R., Cui Q.Y., Murai K., Lim Y.C., Smith Z.D., Jin S., et al. Tet1 regulates adult hippocampal neurogenesis and cognition. Cell Stem Cell 2013, 13(2):237-245. 10.1016/j.stem.2013.05.006.
242. Zhu B., Zheng Y., Angliker H., Schwarz S., Thiry S., Siegmann M., et al. 5-methylcytosine DNA glycosylase activity is also present in the human MBD4 (G/T mismatch glycosylase) and in a related avian sequence. Nucleic Acids Research 2000, 28(21):4157-4165.
243. Zhu B., Zheng Y., Hess D., Angliker H., Schwarz S., Siegmann M., et al. 5-methylcytosine-DNA glycosylase activity is present in a cloned G/T mismatch DNA glycosylase associated with the chicken embryo DNA demethylation complex. Proceedings of the National Academy of Sciences of the United States of America 2000, 97(10):5135-5139. 10.1073/pnas.100107597.
244. Zhubi A., Veldic M., Puri N.V., Kadriu B., Caruncho H., Loza I., et al. An upregulation of DNA-methyltransferase 1 and 3a expressed in telencephalic GABAergic neurons of schizophrenia patients is also detected in peripheral blood lymphocytes. Schizophrenia Research 2009, 111(1-3):115-122. 10.1016/j.schres.2009.03.020.