Epigenetic GABAergic targets in schizophrenia and bipolar disorder

Neuropharmacology

Volumn 60, Issue 7-8, 2011, Pages 1007-1016

  Guidotti, A ^a   Auta, J ^a   Chen, Y ^a   Davis, J M ^a   Dong, E ^a   Gavin, D P ^a   Grayson, D R ^a   Matrisciano, F ^a   Pinna, G ^a   Satta, R ^a   Sharma, R P ^a   Tremolizzo, L ^a   Tueting, P ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Chromatin; DNA methyltransferase (DNMT); Glutamic acid decarboxylase 67 (GAD67); Histone deacetylase (HDAC); Promoter methylation; Valproic acid (VPA)

Indexed keywords

4 [2 AMINO 4 (METHYLTHIO)BUTYRYLAMINO] 2 THIABICYCLO[3.1.0]HEXANE 4,6 DICARBOXYLIC ACID 2,2 DIOXIDE; ARIPIPRAZOLE; CATECHOLAMINE RECEPTOR; CLOZAPINE; CLOZAPINE DERIVATIVE; DIBENZEPIN; DNA METHYLTRANSFERASE; GLUTAMIC ACID; HALOPERIDOL; HISTONE DEACETYLASE INHIBITOR; NEUROLEPTIC AGENT; OLANZAPINE; PERPHENAZINE; QUETIAPINE; RISPERIDONE; SEROTONIN RECEPTOR; SULPIRIDE; VALPROIC ACID; APOLIPOPROTEIN E2; BRAIN DERIVED NEUROTROPHIC FACTOR; BUNGAROTOXIN RECEPTOR; GLUTAMATE DECARBOXYLASE 67; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INTEGRIN; METHIONINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; NICOTINIC RECEPTOR ALPHA4; REELIN; VERY LOW DENSITY LIPOPROTEIN;

BINDING AFFINITY; BIPOLAR DISORDER; BRAIN CORTEX; BRAIN DYSFUNCTION; CHROMATIN ASSEMBLY AND DISASSEMBLY; COGNITION; DEMETHYLATION; DISEASE COURSE; DRUG MECHANISM; DRUG POTENTIATION; DRUG RECEPTOR BINDING; DRUG TARGETING; EPIGENETICS; GABAERGIC SYSTEM; GENE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GLUTAMIC ACID DECARBOXYLASE 67 GENE; HIPPOCAMPUS; HUMAN; INTERNEURON; NONHUMAN; PATHOPHYSIOLOGY; PHARMACOGENETICS; PRIORITY JOURNAL; PROMOTER REGION; PYRAMIDAL NERVE CELL; REELIN GENE; REVIEW; SCHIZOPHRENIA; SYMPTOM; CELL INTERACTION; DENDRITIC SPINE; DOWN REGULATION; DRUG ACTIVITY; DRUG EFFICACY; DRUG SAFETY; DRUG STRUCTURE; GABAERGIC GENE; GABAERGIC TRANSMISSION; GENE EXPRESSION; GENE FREQUENCY; GENETIC SUSCEPTIBILITY; IMMUNOPRECIPITATION; MOLECULAR DYNAMICS; NEUROTRANSMISSION; PREFRONTAL CORTEX; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIPSYCHOTIC AGENTS; BIPOLAR DISORDER; EPIGENESIS, GENETIC; EXCITATORY AMINO ACID AGENTS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION; HUMANS; INTERNEURONS; MICE; MOLECULAR TARGETED THERAPY; SCHIZOPHRENIA;

EID: 79954612114     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2010.10.021     Document Type: Review

References (89)

1. H.M. Abdolmaleky, K.H. Cheng, A. Russo, C.L. Smith, S.V. Faraone, M. Wilcox, R. Shafa, S.J. Glatt, G. Nguyen, J.F. Ponte, S. Thiagalingam, and M.T. Tsuang Hypermethylation of the reelin (RELN) promoter in the brain of schizophrenic patients: a preliminary report Am. J. Med. Genet. B Neuropsychiatr. Genet. 134B 2005 60 66 (Pubitemid 40411111)
2. S. Akbarian, J.J. Kim, S.G. Potkin, J.O. Hagman, A. Tafazzoli, W.E. Bunney Jr., and E.G. Jones Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics Arch. Gen. Psychiatry 52 1995 258 266
3. J.M. Alarcón, G. Malleret, K. Touzani, S. Vronskaya, S. Ishii, E.R. Kandel, and A. Barco Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration Neuron 42 2004 947 959 (Pubitemid 38798233)
4. J.E. Belforte, V. Zsiros, E.R. Sklar, Z. Jiang, G. Yu, Y. Li, E.M. Quinlan, and K. Nakazawa Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes Nat. Neurosci. 12 2010 76 83
5. F.M. Benes, and S. Beretta GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder Neuropsychopharmacology 25 2001 1 27 (Pubitemid 32493819)
6. A receptor binding in superficial layers of cingulate cortex in schizophrenics J. Neurosci. 12 1992 924 929
7. F.M. Benes, B. Lim, D. Matzilevich, J.P. Walsh, S. Subburaju, and M. Minns Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars Proc. Natl. Acad. Sci. U.S.A. 104 2007 10164 10169 (Pubitemid 47175280)
8. B.K.Y. Bitanihirwe, M.P. Lim, J.F. Kelley, T. Kaneko, and T.U.W. Woo Glutamatergic deficits and parvalbumin-containing inhibitory neurons in the prefrontal cortex in schizophrenia BMC Psychiatry 9 2009 71
9. C.R. Breese, M.J. Lee, C.E. Adams, B. Sullivan, J. Logel, K.M. Gillen, M.J. Marks, A.C. Collins, and S. Leonard Abnormal regulation of high affinity nicotinic receptors in subjects with schizophrenia Neuropsychopharmacology 23 2000 351 364
10. J.L. Browning, T. Patel, P.C. Brandt, K.A. Young, L.A. Holcomb, and P.B. Hicks Clozapine and the mitogen-activated protein kinase signal transduction pathway: implications for antipsychotic actions Biol. Psychiatry 57 2005 617 623 (Pubitemid 40409701)
11. D.E. Casey, D.G. Daniel, C. Tamminga, J.M. Kane, T. Tran-Johnson, P. Wozniak, W. Abi-Saab, J. Baker, L. Redden, N. Greco, and M. Saltarelli Divalproex ER combined with olanzapine or risperidone for treatment of acute exacerbations of schizophrenia Neuropsychopharmacology 3 Dec. 2008 10.1038/npp.2008.209
12. Y. Chen, M. Kundakovic, R.C. Agis-Balboa, G. Pinna, and D.R. Grayson Induction of the reelin promoter by retinoic acid is mediated by Sp1 J. Neurochem. 183 2007 650 665 (Pubitemid 47498032)
13. 1 promoter: trans-acting factors and DNA methylation converge on the 5′ untranslated region Neuropharmacology 2010 Sept. 27 (Epub ahead of print, PMID20869372)
14. D.M. Chuang, Y. Leng, Z. Marinova, H.J. Kim, and C.T. Chiu Multiple roles of HDAC inhibition in neurodegenerative conditions Trends Neurosci. 32 2009 591 601
15. E. Costa, J. Davis, D.R. Grayson, A. Guidotti, G.D. Pappas, and C. Pesold Dendritic spine hypoplasticity and downregulation of reelin and GABAergic tone in schizophrenia vulnerability Neurobiol. Dis. 8 2001 723 742 (Pubitemid 33055591)
16. E. Costa, Y. Chen, J. Davis, E. Dong, J.S. Noh, L. Tremolizzo, M. Veldic, D.R. Grayson, and A. Guidotti Reelin and schizophrenia: a disease at the interface of the genome and the epigenome Mol. Interv. 2002 47 57 2002
17. E. Costa, E. Dong, D.R. Grayson, A. Guidotti, W. Ruzicka, and M. Veldic Reviewing the role of DNA (cytosine-5) methyltransferase overexpression in the cortical GABAergic dysfunction associated with psychosis vulnerability Epigenetics 2 2007 29 36 (Pubitemid 46824847)
18. N. Detich, V. Bovenzi, and M. Szyf Valproate induces replication- independent active DNA demethylation J. Biol. Chem. 278 2003 27586 27592 (Pubitemid 36899944)
19. 67 promoter remodeling in an epigenetic methionine-induced mouse model of schizophrenia Proc. Natl. Acad. Sci. U.S.A. 102 2005 12578 12583 (Pubitemid 41266401)
20. E. Dong, A. Guidotti, D.R. Grayson, and E. Costa Histone hyperacetylation induces demethylation of reelin and 67-kDa glutamic acid decarboxylase promoters Proc. Natl. Acad. Sci. U.S.A. 104 2007 4676 4681 (Pubitemid 47186284)
21. E. Dong, M. Nelson, D.R. Grayson, E. Costa, and A. Guidotti Clozapine and sulpiride but not haloperidol or olanzapine activate nuclear DNA-demethylation in the brain Proc. Natl. Acad. Sci. U.S.A. 105 2008 13614 13619
22. E. Dong, Y. Chen, D.P. Gavin, D.R. Grayson, and A. Guidotti Valproate induces DNA demethylation in nuclear extracts from adult mouse brain Epigenetics 5 8 Nov. 16 2010 730 735
23. 65 mRNA and protein expression in cerebrocortical regions of elderly patients with schizophrenia J. Neurosci. Res. 76 2004 581 592 (Pubitemid 38580473)
24. S.L. Eastwood, and P. Harrison Decreased expression of vesicular glutamate transporter 1 and complexin II mRNAs in schizophrenia: further evidence for a synaptic pathology affecting glutamate neurons Schizophr. Res. 73 2005 159 172 (Pubitemid 40093877)
25. S.H. Fatemi, J.A. Earle, and T. McMenomy Reduction in reelin immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorder and major depression Mol. Psychiatry 5 2000 654 665
26. D.P. Gavin, K. Chase, F. Matrisciano, D.R. Grayson, A. Guidotti, and R.P. Sharma Growth Arrest and DNA-Damage-Inducible, Beta (GADD45b) Expression and Function in the Brain: An Examination of a Putative Member of a DNA Demethylation Pathway Abnormally Expressed in Psychosis 2010 Society for Neuroscience Abstract
27. J.A. Gray, and B.L. Roth The pipeline and future of drug development in schizophrenia Mol. Psychiatry 12 2007 904 922 (Pubitemid 47482704)
28. D.R. Grayson, X. Jia, Y. Chen, R.P. Sharma, C.O. Mitchell, A. Guidotti, and E. Costa Reelin promoter hypermethylation in schizophrenia Proc. Natl. Acad. Sci. U.S.A. 102 2005 9341 9346 (Pubitemid 40923565)
29. D.R. Grayson, Y. Chen, E. Costa, E. Dong, A. Guidotti, M. Kundakovic, and R.P. Sharma The human reelin gene: transcription factors (+), repressors (-) and the methylation switch (+/-) in schizophrenia Pharmacol. Ther. 111 2006 272 286 (Pubitemid 43765535)
30. 67) expression in schizophrenia and bipolar disorder: a postmortem brain study Arch. Gen. Psychiatry 57 2000 1061 1069
31. A. Guidotti, J. Auta, J.M. Davis, E. Dong, D.R. Grayson, M. Veldic, X. Zhang, and E. Costa GABAergic dysfunction in schizophrenia: new treatment strategies on the horizon Psychopharmacology 180 2005 191 205 (Pubitemid 40909664)
32. A. Guidotti, W. Ruzicka, D.R. Grayson, M. Veldic, G. Pinna, J.M. Davis, and E. Costa S-adenosyl methionine and DNA methyltransferase-1 mRNA overexpression in psychosis Neuroreport 18 2007 57 60 (Pubitemid 46183390)
33. A. Guidotti, E. Dong, M. Kundakovic, R. Satta, D.R. Grayson, and E. Costa Characterization of the action of antipsychotic subtypes on valproate-induced chromatin remodeling Trends Pharmacol. Sci. 30 2009 55 60
34. J.J. Hill, N. Kolluri, T. Hashimoto, Q. Wu, A.R. Sampson, and L.M. Monteggia Analysis of pyramidal neuron morphology in an inducible knockout of brain derived neurotrophic factors Biol. Psychiatry 57 2005 923 934
35. H.S. Huang, A. Matevossian, C. Whittle, S.Y. Kim, A. Shumacker, S.P. Baker, and S. Akbarian Prefrontal dysfunction in schizophrenia involves mixed-lineage leukemia 1-regulated histone methylation at GABAergic gene promoters J. Neurosci. 27 2007 11254 11262 (Pubitemid 47621326)
36. F. Impagnatiello, A. Guidotti, C. Pesold, Y. Dwivedi, H. Caruncho, M. Pisu, D. Uzunov, N. Smalheiser, J. Davis, G. Pandey, G. Pappas, P. Tueting, R. Sharma, and E. Costa A decrease of reelin expression as a putative vulnerability factor in schizophrenia Proc. Natl. Acad. Sci. U.S.A. 95 1998 15718 15723 (Pubitemid 29018766)
37. L.F. Jarskog, S. Miyamoto, and J.A. Lieberman Schizophrenia: new pathological insights and therapies Annu. Rev. Med. 58 2007 49 61 (Pubitemid 46706500)
38. T. Jenuwein, and C.D. Allis Translating the histone code Science 293 2001 1074 1080 (Pubitemid 32758077)
39. D.L. Kelly, R.R. Conley, S. Feldman, Y. Yu, R.P. McMahon, and C.M. Richardson Adjunct divalproex or lithium to clozapine in treatment-resistant schizophrenia Psychiatr. Q. 77 2006 81 95 (Pubitemid 43060798)
40. M.S. Kim, T. Kondo, I. Takada, M.Y. Youn, Y. Yamamoto, S. Takahashi, T. Matsumoto, S. Fujiyama, Y. Shirode, I. Yamaoka, H. Kitagawa, K. Takeyama, H. Shibuya, F. Ohtake, and S. Kato DNA demethylation in hormone-induced transcriptional derepression Nature 461 2009 1007 1012
41. 67 promoters are activated by epigenetic drugs that facilitate the disruption of local repressor complexes Mol. Pharmacol. 75 2009 342 354
42. J.M. Levenson, K.J. O'Riordan, K.D. Brown, M.A. Trinh, D.L. Molfese, and J.D. Sweatt Regulation of histone acetylation during memory formation in the hippocampus J. Biol. Chem. 279 2004 40545 40559 (Pubitemid 39287646)
43. J.M. Levenson, S. Qiu, and E.F. Weeber The role of reelin in adult synaptic function and the genetic and epigenetic regulation of the reelin gene Biochim. Biophys. Acta 1779 2008 422 431
44. D.A. Lewis, and G. González-Burgos Neuroplasticity of neocortical circuits in schizophrenia Neuropsychopharmacology 33 2008 141 165 (Pubitemid 350191315)
45. D.A. Lewis, T. Hashimoto, and D.W. Volk Cortical inhibitory neurons and schizophrenia Nat. Rev. Neurosci. 6 2005 312 324 (Pubitemid 40469985)
46. M.D. Li Grand challenges and opportunities for molecular psychiatry research: a perspective Front. Psychiatry 1 2 2010 1 3 10.3389/fpsyt.2010.00002
47. B.K. Lipska, T. Peters, T.M. Hyde, N. Halim, C. Horowitz, and S. Mitkus Expression of DISC1 binding partners is reduced in schizophrenia and is associated with DSC1 SNPs Hum. Mol. Genet. 15 2006 1245 1258
48. J.E. Lisman, J.T. Coyle, R.W. Green, D.C. Javitt, F.M. Benes, S. Heckers, and A.A. Grace Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia Trends Neurosci. 31 2008 234 242
49. W. Loscher Valproate: a reappraisal of its pharmacodynamic properties and mechanisms of action Prog. Neurobiol. 58 1999 31 59 (Pubitemid 29166878)
50. D.K. Ma, M.H. Jang, J.U. Guo, Y. Kitabatake, M.L. Chang, N. Pow-Anpongkul, R.A. Flavell, B. Lu, G.L. Ming, and H. Song Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis Science 323 2009 1074 1077
51. A.K. McAllister, L.C. Katz, and D.C. Lo Neurotrophin regulation of cortical dendritic growth requires activity Neuron 17 1996 1057 1064 (Pubitemid 27021093)
52. J. Mill, T. Tang, Z. Kaminsky, T. Khare, S. Yazdanpanah, L. Bouchard, P. Jia, A. Assadzadeh, J. Flanagan, A. Schumacher, S.C. Wang, and A. Petronis Epigenomic profiling reveals DNA-methylation changes associated with major psychosis Am. J. Hum. Genet. 82 2008 696 711 (Pubitemid 351726115)
53. G. Miller Is pharma running out of brainy ideas? Science 329 2010 502 504
54. C.A. Miller, and J.D. Sweatt Covalent modification of DNA regulates memory formation Neuron 1533 2007 857 869 (Pubitemid 46367557)
55. C.A. Miller, C.F. Gavin, J.A. White, R.R. Parrish, A. Honasoge, C.R. Yancey, I.M. Rivera, M.D. Rubio, G. Rumbaugh, and J.D. Sweatt Cortical DNA methylation maintains remote memory Nat. Neurosci. 13 2010 664 666
56. C.P. Mitchell, Y. Chen, M. Kundakovic, E. Costa, and D.R. Grayson Histone deacetylase inhibitors decrease reelin promoter methylation in vitro J. Neurochem. 93 2005 483 492 (Pubitemid 40547505)
57. B. Moghaddam Bringing order to the glutamate chaos in schizophrenia Neuron 20 2003 881 884 (Pubitemid 37522046)
58. J.S. Noh, R.P. Sharma, M. Veldic, A.A. Salvacion, X. Jia, Y. Chen, E. Costa, and A. Guidotti DNA methyltransferase 1 regulates reelin mRNA expression in mouse primary cortical cultures Proc. Natl. Acad. Sci. U.S.A. 102 2005 1749 1754 (Pubitemid 40209239)
59. S.K.T. Ooi, and T.H. Bestor The colorful history of active DNA demethylation Cell 133 2008 145 148
60. S. Peleg, F. Sananbenesi, A. Zovoilis, S. Burkhardt, S. Bahari-Javan, R.C. Agis-Balboa, P. Cota, J.L. Wittnam, A. Gogol-Doering, L. Opitz, G. Salinas-Riester, M. Dettenhofer, H. Kang, L. Farinelli, W. Chen, and A. Fischer Altered histone acetylation is associated with age-dependent memory impairment in mice Science 328 2010 753 756
61. C. Ptak, and A. Petronis Epigenetics and complex disease: from etiology to new therapeutics Annu. Rev. Pharmacol. Toxicol. 48 2008 257 276 (Pubitemid 351738154)
62. L. Pujadas, A. Gruart, C. Bosch, L. Delgado, C. Teixeira, D. Rossi, L. deLecea, A. Martinez, J.M. Delgado-Garcia, and E. Soriano Reelin regulates postnatal neurogenesis and enhances spine hypertrophy and long-term potentiation J. Neurosci. 30 2010 4636 4649
63. A. Razin, and R. Shemer DNA methylation in early development Hum. Mol. Genet. 4 1995 1751 1755
64. B.L. Roth, D.J. Sheffler, and W.K. Kroeze Magic shotguns versus magic bullets: selectively non-selective drugs for mood disorders and schizophrenia Nat. Rev. Drug Discov. 3 2004 353 359 (Pubitemid 38499762)
65. T.L. Roth, F.D. Lubin, M. Sodhi, and J.E. Kleinman Epigenetic mechanisms in schizophrenia Biochem. Biophys. Acta 1790 2009 869 877
66. W.B. Ruzicka, A. Zhubi, M. Veldic, D.R. Grayson, E. Costa, and A. Guidotti Selective epigenetic alteration of layer I GABAergic neurons isolated from prefrontal cortex of schizophrenia patients using laser-assisted microdissection Mol. Psychiatry 12 2007 385 397 (Pubitemid 46496836)
67. R. Satta, E. Maloku, A. Zhubi, F. Pibiri, M. Hajos, E. Costa, and A. Guidotti Nicotine targets the epigenetic mechanisms in selected populations of mouse telencephalic GABAergic neurons Proc. Natl. Acad. Sci. U.S.A. 105 2008 16356 16361
68. R.P. Sharma, D.R. Grayson, and D.P. Gavin Histone deacetylase 1 expression is increased in the prefrontal cortex of schizophrenia subjects: analysis of the National Brain Databank microarray collection Schizophr. Res. 98 2008 111 117 (Pubitemid 350235899)
69. S. Shifman, M. Johannesson, M. Bronstein, S.X. Chen, D.A. Collier, N.J. Craddock, K.S. Kendler, T. Li, M. O'Donovan, F.A. O'Neill, M.J. Owen, D. Walsh, D.R. Weinberger, C. Sun, J. Flint, and A. Darvasi Genome-wide association identifies a common variant in the reelin gene that increases the risk of schizophrenia only in women PLoS Genet. 4 2008 e28
70. M.V. Simonini, L.M. Camargo, E. Dong, E. Maloku, M. Veldic, E. Costa, and A. Guidotti The benzamide MS-275 is a potent long-lasting brain region-selective inhibitor of histone deacetylases Proc. Natl. Acad. Sci. U.S.A. 103 2006 1587 1592 (Pubitemid 43191209)
71. 67) is associated with schizophrenia and influences cortical function and gene expression Mol. Psychiatry 12 2007 854 869 (Pubitemid 47347790)
72. P.F. Sullivan, D. Lin, J.Y. Tzeng, E. van den Oord, D. Perkins, T.S. Stroup, M. Wagner, S. Lee, F.A. Wright, F. Zou, W. Liu, A.M. Downing, J. Lieberman, and S.L. Close Genomewide association for schizophrenia in the CATIE study: results of stage 1 Mol. Psychiatry 13 2008 570 584 (Pubitemid 351704941)
73. M. Szyf DNA methylation and demethylation as targets for anticancer therapy Biochemistry (Mosc.) 70 2005 533 544
74. L. Tremolizzo, M.-S. Doueiri, E. Dong, D.R. Grayson, J. Davis, G. Pinna, P. Tueting, V. Rodriguez-Menendez, E. Costa, and A. Guidotti Valproate corrects the schizophrenia-like epigenetic behavioral modifications induced by methionine in mice Biol. Psychiatry 57 2005 500 509 (Pubitemid 40311985)
75. L. Tremolizzo, G. Carboni, W.B. Ruzicka, C.P. Mitchell, I. Sugaya, P. Tueting, R. Sharma, D.R. Grayson, E. Costa, and A. Guidotti An epigenetic mouse model for molecular and behavioral neuropathologies related to schizophrenia vulnerability Proc. Natl. Acad. Sci. U.S.A 99 2002 17095 17100 (Pubitemid 36034104)
76. P. Tueting, E. Costa, Y. Dwivedi, A. Guidotti, F. Impagnatiello, R. Manev, and C. Pesold The phenotypic characteristics of heterozygous reeler mouse Neuroreport 10 1999 1329 1334 (Pubitemid 29403718)
77. P. Tueting, J.M. Davis, M. Veldic, F. Pibiri, B. Kadriu, A. Guidotti, and E. Costa L-methionine decreases dendritic spine density in mouse frontal cortex Neuroreport 21 2010 543 548 2010
78. B.O. Van Emburgh, and K.D. Robertson DNA methyltransferases and methyl CpG binding proteins as multifunctional regulators of chromatin structure and development in mammalian cells J. Tost, Epigenetics 2008 Caister Academic Press Norwich, UK 23 62
79. M. Veldic, J.H. Caruncho, W.S. Liu, J. Davis, R. Satta, D.R. Grayson, A. Guidotti, and E. Costa DNA methyltransferase-1 (DNMT1) is selectively overexpressed in telencephalic GABAergic interneurons of schizophrenia brains Proc. Natl. Acad. Sci. U.S.A. 101 2004 348 353 (Pubitemid 38084253)
80. M. Veldic, A. Guidotti, E. Maloku, J.M. Davis, and E. Costa In psychosis, cortical interneurons overexpress DNA-methyltransferase 1 Proc. Natl. Acad. Sci. U.S.A. 102 2005 2152 2157 (Pubitemid 40262027)
81. M. Veldic, B. Kadriu, E. Maloku, R.C. Agis-Balboa, A. Guidotti, J.M. Davis, and E. Costa Epigenetic mechanisms expressed in basal ganglia GABAergic neurons differentiate schizophrenia from bipolar disorder Schizophr. Res. 91 2007 51 61
82. A.A. Wassef, S.G. Dott, A. Harris, A. Brown, M. O'Boyle, W.J. Meyer 3rd, and R.M. Rose Randomized, placebo-controlled pilot study of divalproex sodium in the treatment of acute exacerbations of chronic schizophrenia J. Clin. Psychopharmacol. 20 2000 357 361 (Pubitemid 30318366)
83. I.C. Weaver, M.J. Meaney, and M. Szyf Maternal care effects on the hippocampal transcriptome and anxiety mediated behaviors in the offspring that are reversible in the adulthood Proc. Natl. Acad. Sci. U.S.A. 103 2006 3480 3485 (Pubitemid 43346494)
84. J. Wedenoja, A. Loukola, A. Tuulio-Henriksson, T. Paunio, J. Ekelund, K. Silander, T. Varilo, K. Heikkilä, J. Suvisaari, T. Partonen, J. Lönnqvist, and L. Peltonen Replication of linkage on chromosome 7q22 and association of the regional Reelin gene with working memory in schizophrenia families Mol. Psychiatry 13 2008 673 684 (Pubitemid 351861527)
85. 2A in the anterior cingulate cortex in schizophrenia and bipolar disorder Arch. Gen. Psychiatry 61 2004 649 657 (Pubitemid 38890797)
86. T.-U. Woo, K. Shrestha, D. Lamb, M.M. Minns, and F.M. Benes N-methyl-d-aspartate receptor and calbindin-containing neurons in the anterior cingulate cortex in schizophrenia and bipolar disorder Biol. Psychiatry 64 2008 803 809
87. R.J. Wyatt, B.A. Termini, and J. Davis Biochemical and sleep studies of schizophrenia. A review of the literature 1960-1970 Schizophr. Bull. 4 1971 10 44
88. J.K. Zhu Active DNA demethylation mediated by DNA glycosylases Annu. Rev. Genet. 43 2009 143 166
89. A. Zhubi, M. Veldic, N.V. Puri, B. Kadriu, H. Caruncho, I. Loza, H. Sershen, A. Lajtah, R.C. Smith, A. Guidotti, J.M. Davis, and E. Costa An upregulation of DNA-methyltransferase 1 and 3a expressed in telencephalic GABAergic neurons of schizophrenia patients is also detected in peripheral blood lymphocytes Schizophr. Res. 111 2009 115 122