The human reelin gene: Transcription factors (+), repressors (-) and the methylation switch (+/-) in schizophrenia

Pharmacology and Therapeutics

Volumn 111, Issue 1, 2006, Pages 272-286

  Grayson, Dennis R ^a   Chen, Ying ^a   Costa, Erminio ^a   Dong, Erbo ^a   Guidotti, Alessandro ^a   Kundakovic, Marija ^a   Sharma, Rajiv P ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

AZA; azadeoxycytidine; bipolar disorder; BP; DNA methyltransferase; Dnmt; Drug development; GABA; GAD; gamma amino butyric acid; Gene; Glutamate decarboxylase; glutamic acid decarboxylase; HDAC; heterochromatin protein 1; histone deacetylase; Histone deacetylase; HP1; long term potentiation; LTP; MBD2; MeCP2; methyl binding domain protein 2; methyl CPG binding protein 2; Methylation; Migration; Neuron; Promoter; Psychiatry; Schizophrenia; schizophrenia; Simian virus 40; SV40; SZ; Trichostatin A; TSA; valproic acid; VPA

Indexed keywords

4 AMINOBUTYRIC ACID; DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE INHIBITOR; GLUTAMATE DECARBOXYLASE; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; MESSENGER RNA; REELIN; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR;

AUTOPSY; BIPOLAR DISORDER; BRAIN REGION; CELL LINE; CENTRAL NERVOUS SYSTEM; CHROMATIN STRUCTURE; DOWN REGULATION; DRUG INHIBITION; EPIGENETICS; GENE DELETION; GENE OVEREXPRESSION; GENE STRUCTURE; GENETIC ANALYSIS; GENETIC TRANSFECTION; HUMAN; MAJOR DEPRESSION; METHYLATION; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REVIEW; SCHIZOPHRENIA; SYMPTOMATOLOGY;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CENTRAL NERVOUS SYSTEM; DNA METHYLATION; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION; GLUTAMATE DECARBOXYLASE; HUMANS; ISOENZYMES; NERVE TISSUE PROTEINS; NEURONS; PROMOTER REGIONS (GENETICS); REPRESSOR PROTEINS; RNA, MESSENGER; SCHIZOPHRENIA; SERINE ENDOPEPTIDASES; TRANSCRIPTION FACTORS;

EID: 33646757886     PISSN: 01637258     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2005.01.007     Document Type: Review

References (133)

1. 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. Am J Med Genet B Neuropsychiatr Genet 134 (2005) 60-66
2. Ahringer J. NuRD and SIN3 histone deacetylase complexes in development. Trends Genet 16 (2000) 351-356
3. 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. Arch Gen Psychiatry 62 (2005) 829-840
4. Alcantara S., Ruiz M., D'Arcangelo G., Ezan F., de Lecea L., Curran T., et al. Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci 18 (1998) 7779-7799
5. Amir R.E., and Zoghbi H.Y. Rett syndrome: methyl-CpG-binding protein 2 mutations and phenotype-genotype correlations. Am J Med Genet 97 (2000) 147-152
6. Amir R.E., Van den Veyver I.B., Wan M., Tran C.Q., Francke U., and Zoghbi H.Y. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23 (1999) 185-188
7. Antun F.T., Burnett G.B., Cooper A.J., Daly R.J., Smythies J.R., and Zealley A.K. The effects of l-methionine (without MAOI) in schizophrenia. J Psychiatry Res 8 (1971) 63-71
8. Beffert U., Weeber E.J., Durudas A., Qiu S., Masilius I., Sweatt J.D., et al. Modulation of synaptic plasticity and memory by reelin involves differential splicing of the lipoprotein receptor Apoer2. Neuron 47 (2005) 567-579
9. Benes F.M., and Berretta S. GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology 25 (2001) 1-27
10. Benes F.M., Vincent S.L., Alsterberg G., Bird E.D., and SanGiovanni J.P. Increased GABAA receptor binding in superficial layers of cingulate cortex in schizophrenics. J Neurosci 12 (1992) 924-929
11. Benes F.M., Vincent S.L., Marie A., and Khan Y. Up-regulation of GABAA receptor binding on neurons of the prefrontal cortex in schizophrenic subjects. Neuroscience 75 (1996) 1021-1031
12. Biel M., Wascholowski V., and Giannis A. Epigenetics-an epicenter of gene regulation: histones and histone-modifying enzymes. Angew Chem Int Ed Engl 44 (2005) 3186-3216
13. Bowen N.J., Palmer M.B., and Wade P.A. Chromosomal regulation by MeCP2: structural and enzymatic considerations. Cell Mol Life Sci 61 (2004) 2163-2167
14. Bulfone A., Smiga S.M., Shimamura K., Peterson A., Puelles L., and Rubenstein J.L. T-brain-1: a homologue of Brachyury whose expression defines molecularly distinct domains within the cerebral cortex. Neuron 15 (1995) 63-78
15. Burgers W.A., Fuks F., and Kouzarides T. DNA methyltransferases get connected to chromatin. Trends Genet 18 (2002) 275-277
16. Caballero I.M., and Hendrich B. MeCP2 in neurons: closing in on the cause of Rett syndrome. Hum Mol Genet 14 (2005) R19-R26
17. Carboni G., Tueting P., Tremolizzo L., Sugaya I., Davis J., Costa E., et al. Enhanced dizocilpine efficacy in heterozygous reeler mice relates to GABA turnover downregulation. Neuropharmacology 46 (2004) 1070-1081
18. Cervoni N., and Szyf M. Demethylase activity is directed by histone acetylation. J Biol Chem 276 (2001) 40778-40787
19. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J 10 (1996) 940-954
20. Chen R.Z., Akbarian S., Tudor M., and Jaenisch R. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat Genet 27 (2001) 327-331
21. Chen Y., Sharma R.P., Costa R.H., Costa E., and Grayson D.R. On the epigenetic regulation of the human reelin promoter. Nucleic Acids Res 30 (2002) 2930-2939
22. Chen, Y., Costa, E., & Grayson, D. R. (2004). Regulation of human reelin by Pax6, Tbr1 and Sp1 in neuronal precursor cells. Program No. 909.3 Abstract viewer/itinerary planner. Washington, DC: Soc for Neurosci 2004 online.
23. Chu S., and Ferro T.J. Sp1: regulation of gene expression by phosphorylation. Gene 348 (2005) 1-11
24. Costa E., Davis J., Grayson D.R., Guidotti A., Pappas G.D., and Pesold C. Reelin downregulation and dendritic spine hypoplasia as putative vulnerability factors in schizophrenia. Neurobiol Dis 8 (2001) 723-742
25. Costa E., Chen Y., Davis J., Dong E., Noh J.S., Tremolizzo L., et al. REELIN and schizophrenia: a disease at the interface of the genome and the epigenome. Mol Interv 2 (2002) 47-57
26. Costa E., Grayson D.R., and Guidotti A. Epigenetic downregulation of GABAergic function in schizophrenia: potential for pharmacological intervention?. Mol Interv 3 (2003) 200-229
27. Costa E., Grayson D.R., Mitchell C.P., Tremolizzo L., Veldic M., and Guidotti A. GABAergic cortical neuron chromatin as a putative target to treat schizophrenia vulnerability. Crit Rev Neurobiol 15 (2003) 121-142
28. Costa E., Grayson D.R., Veldic M., and Guidotti A. Neurochemical basis for an epigenetic vision of synaptic organization. Int Rev Neurobiol 59 (2004) 73-91
29. Costello J.F., and Plass C. Methylation matters. J Med Genet 38 (2001) 285-303
30. Curran T., and D'Arcangelo G. Role of reelin in the control of brain development. Brain Res Brain Res Rev 26 (1998) 285-294
31. D'Arcangelo G. Apoer2: a reelin receptor to remember. Neuron 47 (2005) 471-477
32. D'Arcangelo G., Miao G.G., Chen S.C., Soares H.D., Morgan J.I., and Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374 (1995) 719-723
33. De Bergeyck V., Nakajima K., Lambert de Rouvroit C., Naerhuyzen B., Goffinet A.M., Miyata T., et al. A truncated reelin protein is produced but not secreted in the 'Orleans' reeler mutation (Relnrl-Orl). Mol Brain Res 50 (1997) 85-90
34. DeSilva U., D'Arcangelo G., Braden V.V., Chen J., Miao G.G., Curran T., et al. The human reelin gene: isolation, sequencing, and mapping on chromosome 7. Genome Res 7 (1997) 157-164
35. Detich N., Bovenzi V., and Szyf M. Valproate induces replication-independent active DNA demethylation. J Biol Chem 278 (2003) 27586-27592
36. Dong E., Caruncho H., Liu W.S., Smalheiser N.R., Grayson D.R., Costa E., et al. A reelin-integrin receptor interaction regulates Arc mRNA translation in synapto-neurosomes. Proc Natl Acad Sci U S A 100 (2003) 5479-5484
37. Dong E., Agis-Balboa R.C., Simonini M.V., Grayson D.R., Costa E., and Guidotti A. Reelin and glutamic acid decarboxylase67 promoter remodeling in an epigenetic methionine-induced mouse model of schizophrenia. Proc Natl Acad Sci U S A 102 (2005) 12578-12583
38. Dulabon L., Olson E.C., Taglienti M.G., Eisenhuth S., McGrath B., Walsh C.A., et al. Reelin binds alpha3beta1 integrin and inhibits neuronal migration. Neuron 27 (2000) 33-44
39. Eastwood S.L., and Harrison P.J. Interstioal white matter neurons express less reelin and are abnormally distributed in schizophrenia: towards an integration of molecular and morphologic aspects of the neurodevelopmental hypothesis. Mol Psychiatry 8 (2003) 821-831
40. El-Osta A. Dnmt cooperativity-the developing links between methylation, chromatin structure and cancer. BioEssays 25 (2003) 1071-1084
41. Fan G., and Hutnick L. Methyl-CpG binding proteins in the nervous system. Cell Res 15 (2005) 255-261
42. Fan G., Beard C., Chen R.Z., Csankovszki G., Sun Y., Siniaia M., et al. DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. J Neurosci 21 (2001) 788-797
43. Fatemi S.H., Earle J.A., and McMenomy T. Reduction in reelin immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorder and major depression. Mol Psychiatry 5 (2000) 654-663
44. Fatemi S.H., Snow A.V., Stary J.M., Araghi-Niknam M., Reutiman T.J., Lee S., et al. Reelin signaling is impaired in autism. Biol Psychiatry 57 (2005) 777-787
45. Fatemi S.H., Stary J.M., Earle J.A., Araghi-Niknam M., and Eagan E. GABAergic dysfunction in schizophrenia and mood disorders as reflected by decreased levels of glutamic acid decarboxylase 65 and 67 kDa and reelin proteins in cerebellum. Schizophr Res 72 (2005) 109-122
46. Fuks F., Burgers W.A., Brehm A., Hughes-Davies L., and Kouzarides T. DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat Genet 24 (2000) 88-91
47. Fuks F., Hurd P.J., Deplus R., and Kouzarides T. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res 31 (2003) 2305-2312
48. Gajovic S., St-Onge L., Yokota Y., and Gruss P. Retinoic acid mediates Pax6 expression during in vitro differentiation of embryonic stem cells. Differentiation 62 (1997) 187-192
49. Gardiner-Garden M., and Frommer M. CpG islands in vertebrate genomes. J Mol Biol 196 (1987) 261-282
50. Glantz L.A., and Lewis D.A. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizphrenia. Arch Gen Psychiatry 57 (2001) 65-73
51. Goll M.G., and Bestor T.H. Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74 (2005) 481-514
52. Grayson D.R., Costa R.H., Xanthopoulos K.G., and Darnell Jr. J.E. A cell-specific enhancer of the mouse α1-antitrypsin gene has multiple functional regions and corresponding protein binding sites. Mol Cell Biol 8 (1988) 1055-1066
53. Grayson D.R., Jia X., Chen Y., Sharma R.P., Mitchell C.P., Guidotti A., et al. Reelin promoter hypermethylation in schizophrenia. Proc Natl Acad Sci U S A 102 (2005) 9341-9346
54. Guidotti A., Auta J., Davis J.M., Di Giorgi-Gerenini V., Dwivedi Y., Grayson D.R., et al. Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch Gen Psychiatry 57 (2000) 1061-1069
55. Guidotti A., Auta J., Davis J.M., Dong E., Grayson D.R., Veldic M., et al. GABAergic dysfunction in schizophrenia: new treatment strategies on the horizon. Psychopharmacology 180 (2005) 191-205
56. Harrison S.M., Houzelstein D., Dunwoodie S.L., and Beddington R.S.P. Sp5, a new member of the Sp1 family, is dynamically expressed during development and genetically interacts with Brachyury. Dev Biol 227 (2000) 358-372
57. Harwood A.J. Neurodevelopment and mood stabilizers. Curr Mol Med 3 (2003) 472-482
58. Hevner R.F., Shi L., Justice N., Hsueh Y., Sheng M., Smiga S., et al. Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29 (2001) 353-366
59. Hiesberger T., Trommsdorff M., Howell B.W., Goffinet A., Mumby M.C., Cooper J.A., et al. Direct binding of reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24 (1999) 481-489
60. Hong S., Shugart Y.Y., Huang D.T., Shahwan S.A., Grant P.E., Hourihane J.O., et al. Autosomal reessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat Genet 27 (2000) 93-96
61. Howell B.W., Hawkes R., Soriano P., and Cooper J.A. Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 389 (1997) 733-737
62. Howell B.W., Herrick T.M., and Cooper J.A. Reelin-induced tyrosine phosphorylation of disabled 1 during neuronal positioning. Genes Dev 13 (1999) 643-648
63. Huang Y., Doherty J.J., and Dingledine R. Altered histone acetylation at glutamate receptor 2 and brain-derived neurotrophic factor genes is an early event triggered by status epilepticus. J Neurosci 22 (2002) 8422-8428
64. Husmann M., Dragneva Y., Romahn E., and Jehnichen P. Nuclear receptors modulate the interaction of Sp1 and GC-rich DNA via ternary complex formation. Biochem J 352 (2000) 763-772
65. Ikeda Y., and Terashima T. Expression of reelin, the gene responsible for the reeler mutation, in embryonic development and adulthood in the mouse. Dev Dyn 210 (1997) 157-172
66. Impagnatiello F., Guidotti A.R., Pesold C., Dwivedi Y., Caruncho H., Pisu M.G., et al. A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proc Natl Acad Sci U S A 95 (1998) 15718-15723
67. Inano K., Suetake I., Ueda T., Miyake Y., Nakamura M., Okada M., et al. Maintenance-type DNA methyltransferase is highly expressed in post-mitotic neurons and localized in the cytoplasmic compartment. J Biochem (Tokyo) 128 (2000) 315-321
68. Jones P.L., Veenstra G.J., Wade P.A., Vermaak D., Kass S.U., Landsberger N., et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 19 (1998) 187-191
69. Kato T., Iwamoto K., Kakiuchi C., Kuratomi G., and Okazaki Y. Genetic or epigeneitc difference causing discordance between monozygotic twins as a clue to molecular basis of mental disorders. Mol Psychiatry 10 (2005) 622-630
70. Katoh M. Regulation of WNT signaling molecules by retinoic acid during neuronal differentiation in NT2 cells: threshold model of WNT action. Int J Mol Med 10 (2002) 683-687
71. Kimura H., and Shiota K. Methyl-CpG-binding protein, MeCP2, is a target molecule for maintenance DNA methyltransferase, Dnmt1. J Biol Chem 278 (2003) 4806-4812
72. Kundakovic M., Chen Y., Costa E., and Grayson D.R. Doxorubicin, acting as a Dnmt1 inhibitor, induces reelin gene expression in neuronal precursor cells. Program No. 912.7 2005 abstract viewer/planner (2005), Soc For Neurosci, Washinton, DC online
73. Lacor P.N., Grayson D.R., Auta J., Sugaya I., Costa E., and Guidotti A. Reelin secretion from glutamatergic neurons in culture is independent from neurotransmitter regulation. Proc Natl Acad Sci U S A 97 (2002) 3556-3561
74. Larson J., Hoffman J.S., Guidotti A., and Costa E. Olfactory learning deficit in heterozygous reeler mice. Brain Res 971 (2003) 40-46
75. Lee L.T.-O., Tan-Un K.-C., Lin M.C.-M., and Chow B.K.-C. Retinoic acid activates human secretin expression by Sp proteins and nuclear factor I in neuronal SH-SY5Y cells. J Neurochem 93 (2005) 339-350
76. Lehrmann E., Hyde T.M., Vawter M.P., Becker K.G., Kleinman J.E., and Freed W.J. The use of microarrays to characterize neuropsychiatric disorders: postmortem studies of substance abuse and schizophrenia. Curr Mol Med 3 (2003) 437-446
77. Leonhardt H., and Cardoso M.C. DNA methylation, nuclear structure, gene expression and cancer. J Cell Biochem Suppl 35 (2000) 78-83
78. Lewis D.A., Hashimoto T., and Volk D.W. Cortical inhibitory neurons and schizophrenia. Nat Neurosci Rev 6 (2005) 312-324
79. Leypoldt F., Lewerenz J., and Methner A. Identification of genes up-regulated by retinoic-acid-induced differentiation of the human neuronal precursor cell line NTERA-2. J Neurochem 76 (2001) 806-814
80. Liu W.S., Pesold C., Rodriguez M.A., Carboni G., Auta J., Lacor P., et al. Down-regulation of dendritic spine and glutamic acid decarboxylase 67 expressions in the reelin haploinsufficient heterozygous reeler mouse. Proc Natl Acad Sci U S A 98 (2001) 3477-3482
81. Maison C., and Almouzni G. HP1 and the dynamics of heterochromatin maintenance. Nat Rev Mol Cell Biol 5 (2004) 296-304
82. Mangelsdorf D.J., and Evans R.M. The RXR heterodimers and orphan receptors. Cell 83 (1995) 841-850
83. Miao G.G., Smeyne R.J., D'Arcangelo G., Copeland N.G., Jenkins N.A., Morgan J.I., et al. Isolation of an allele of reeler by insertional mutagenesis. Proc Natl Acad Sci U S A 91 (1994) 11050-11054
84. Mitchell C.P., Chen Y., Costa E., and Grayson D.R. Histone deacetylase inhibitors decrease reelin promoter methylation in vitro. J Neurochem 93 (2005) 483-492
85. 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 393 (1998) 386-389
86. Newell-Price J., Clark A.J.L., and King P. DNA methylation and silencing of gene expression. TEM 11 (2000) 142-148
87. Noh J.S., Sharma R.P., Veldic M., Salvacion A.A., Jia X., Chen Y., et al. DNA methyltransferase I regulates reelin mRNA expression in mouse primary cortical cultures. Proc Natl Acad Sci U S A 102 (2005) 1749-1754
88. Perlstein W.M., Carter C.S., and Noll D.C. Relation of prefrontal cortex dysfunction to working memory and symptoms in schizophrenics. Am J Psychiatry 158 (2001) 1105-1113
89. Pesold C., Impagnatiello F., Pisu M.G., Uzunov D.P., Costa E., Guidotti A., et al. Reelin is preferentially expressed in neurons synthesizing γ-aminobutyric acid in cortex and hippocampus of adult rats. Proc Natl Acad Sci U S A 95 (1998) 3221-3226
90. 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?. Schizophr Bull 29 (2003) 169-178
91. Phiel C.J., Zhang F., Huang E.Y., Guenther M.G., Lazar M.A., and Klein P.S. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 276 (2001) 36734-36741
92. Pongrac J., Middleton F.A., Lewis D.A., Levitt P., and Mirnics K. Gene expression profiling with DNA microarrays: advancing our understanding of psychiatric disorders. Neurochem Res 27 (2002) 1049-1063
93. Przyborski S.A., Smith S., and Wood A. Transcriptional profiling of neuronal differentiation by human embryonal carcinoma stem cells in vitro. Stem Cells 21 (2003) 459-471
94. Qiu, S., Korwek, K. M., Pratt-Davis, A. R., Peters, M., Bergman, M. Y., & Weeber, E. J. (in press). Cognitive disruption and altered hippocampus synaptic function in Reelin haploinsufficient mice. Neurobiol Learn Mem (electronic publication ahead of print).
95. Ramchandani S., Bhattacharya S.K., Cervoni N., and Szyf M. DNA methylation is a reversible biological signal. Proc Natl Acad Sci U S A 96 (1999) 6107-6112
96. Razin A. CpG methylation, chromatin structure and gene silencing-a three-way connection. EMBO J 17 (1998) 4905-4908
97. Rice D.S., and Curran T. Role of the Reelin signaling pathway in central nervous system development. Annu Rev Neurosci 24 (2001) 1005-1039
98. Robertson K.D. DNA methylation and chromatin-unraveling the tangled web. Oncogene 21 (2002) 5361-5379
99. Robertson K.D. DNA methylation and human disease. Nat Rev Genet 6 (2005) 597-610
100. Robertson K.D., and Wolffe A.P. DNA methylation in health and disease. Nat Rev Genet 1 (2000) 11-19
101. Robertson K.D., Ait-Si-Ali S., Yokochi T., Wade P.A., Jones P.L., and Wolffe A.P. Dnmt1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat Genet 25 (2000) 338-342
102. Rodriguez M., Pesold C., Liu W.S., Kriho V., Guidotti A., Pappas G.D., et al. Colocalization of integrin receptors and reelin in dendritic spine post-synaptic densities of adult non-human primate cortex. Proc Natl Acad Sci U S A 97 (2000) 3556-3561
103. Rosoklija G., Toomayan G., Ellis S.P., Keilp J., Mann J.J., Latov N., et al. Structural abnormalities of subicular dendrites in subjects with schizohprenia and mood disorders: preliminary findings. Arch Gen Psychiatry 57 (2000) 349-356
104. Rountree M.R., Bachman K.E., and Baylin S.B. Dnmt1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat Genet 25 (2000) 269-277
105. Royaux I., Lambert de Rouvroit C., D'Arcangelo G., Demirov D., and Goffinet A.M. Genomic organization of the mouse reelin gene. Genomics 46 (1997) 240-250
106. Safe S., and Kim K. Nuclear-receptor-mediated transactivation through interaction with Sp proteins. Prog Nucleic Acid Res Mol Biol 77 (2004) 1-36
107. Schleimer S.B., Hinton T., Dixon G., and Johnston G.A. GABA transporters GAT-1 and GAT-3 in the human dorsolateral prefrontal cortex in schizophrenia. Neuropsychobiology 50 (2004) 226-230
108. Schmid R.S., Jo R., Shelton S., Kreidberg J.A., and Anton E.S. Reelin, integrin and DAB1 interactions during embryonic cerebral cortical development. Cereb Cortex 15 (2005) 1632-1636
109. Selemon L.D., and Goldman-Rakic P.S. The reduced neuropil hypothesis: a circuit based model of schizophrenia. Biol Psychiatry 45 (1999) 17-25
110. Sharma R.P. Schizophrenia, epigenetics and ligand-activated nuclear receptors: a framework for chromatin therapeutics. Schizophr Res 72 (2005) 79-90
111. Slack A., Cervoni N., Pinard M., and Szyf M. Feedback regulation of DNA methyltransferase gene expression by methylation. Eur J Biochem 264 (1999) 191-199
112. Spencer K.M., Nestor P.G., Perlmutter R., Niznikiewicz M.A., Klump M.C., Frumin M., et al. Neural synchrony indexes disordered perception and cognition in schizophrenia. Proc Natl Acad Sci U S A 101 (2004) 17288-17293
113. Stadler F., Kolb G., Rubusch L., Baker S.P., Jones E.G., and Akbarian S. Histone methylation at gene promoters is associated with developmental regulation and region-specific expression of ionotropic and metabotropic glutamate receptors in human brain. J Neurochem 94 (2005) 324-336
114. Suzuki Y., Shimada J., Shudo K., Matsumura M., Crippa M.P., and Kojima S. Physical interaction between retinoic acid receptor and Sp1: mechanism for induction of urokinase by retinoic acid. Blood 93 (1999) 4264-4276
115. Tarabykin V., Stoykova A., Usman N., and Gruss P. Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development 128 (2001) 1983-1993
116. Tawa R., Ono T., Kurishita A., Okada S., and Hirose S. Changes of DNA methylation level during pre- and postnatal periods in mice. Differentiation 45 (1990) 44-48
117. Torrey E.F., Barci B.M., Webster M.J., Bartko J.J., Meador-Woodruff J.H., and Knable M.B. Neurochemical markers for schizophrenia, bipolar disorder amd major depression in postmortem brains. Biol Psychiatry 57 (2005) 252-260
118. Tremolizzo L., Carboni G., Ruzicka W.B., Mitchell C.P., Sugaya I., Tueting P., et al. An epigenetic mouse model for molecular and behavioral neuropathologies related to schizophrenia vulnerability. Proc Natl Acad Sci U S A 99 (2002) 17095-17100
119. Tremolizzo L., Doueiri M.S., Dong E., Grayson D.R., Davis J., Pinna G., et al. Valproate corrects the schizophrenia-like epigenetic behavioral modifications induced by methinonine in mice. Biol Psychiatry 57 (2005) 500-509
120. Tsujita T., Niikawa N., Yamashita H., Imamura A., Hamada A., Nakane Y., et al. Genomic discordance between monozygotic twins discordant for schizophrenia. Am J Psychiatry 155 (1998) 422-424
121. Tucker K.L. Methylated cytosine and the brain: a new base for neuroscience. Neuron 30 (2001) 649-652
122. Tueting P., Costa E., Dwivedi Y., Guidotti A., Impagnatiello F., Manev R., et al. The phenotypic characteristics of heterozygous reeler mouse. NeuroReport 10 (1999) 1329-1334
123. Uzunov D.P., Grayson D.R., Sharma R., Guidotti A., and Costa E. Reelin (RELN) gene restriction fragment length polymorphism (RFLP) analysis in pedigrees of schizophrenia patients. Abstr Soc Neurosci 25 (1999) 1293 (# 520.2)
124. Vawter M.P., Ferran E., Galke B., Cooper K., Bunney W.E., and Byerley W. Microarray screening of lymphocyte gene expression differences in a multiplex schizophrenia pedigree. Schizophr Res 67 (2004) 41-52
125. 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. Proc Natl Acad Sci U S A 101 (2004) 348-353
126. Veldic M., Guidotti A., Maloku E., Davis J.M., and Costa E. In psychosis, cortical interneurons overexpress DNA-methyltransferase I. Proc Natl Acad Sci U S A 102 (2005) 2152-2157
127. Wade P.A. Methyl CpG-binding proteins and transcriptional repression. BioEssays 23 (2001) 1131-1137
128. Wade P.A., and Wolffe A.P. ReCoGnizing methylated DNA. Nat Struct Biol 8 (2001) 575-577
129. Weaver I.C.G., Champagne F.A., Brown S.E., Dymov S., Sharma S., Meaney M.J., et al. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J Neurosci 25 (2005) 11045-11054
130. Weeber E.J., Beffert U., Jones C., Christian C., Forster E., Sweatt J.D., et al. Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J Biol Chem 277 (2002) 39944-39952
131. Woo T.U., Walsh J.P., and Benes F.M. Density of glutamic acid decarboxylase 67 messenger RNA-containing neurons that express the N-methyl-d-aspartate receptor subunit NR2A in the anterior cingulate cortex in schizophrenia and bipolar disorder. Arch Gen Psychiatry 61 (2004) 649-657
132. Yokochi T., and Robertson K.D. Doxorubicin inhibits Dnmt1, resulting in conditional apoptosis. Mol Pharmacol 66 (2004) 1415-1420
133. Zhang Y., and Reinberg D. Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev 15 (2001) 2343-2360