Analysis of the GAD1 promoter: Trans-acting factors and DNA methylation converge on the 5′ untranslated region

Neuropharmacology

Volumn 60, Issue 7-8, 2011, Pages 1075-1087

  Chen, Ying ^a   Dong, Erbo ^a   Grayson, Dennis R ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Histone deacetylase inhibitors; Interneurons; Methylation; Regulation; Schizophrenia

Indexed keywords

GLUTAMATE DECARBOXYLASE 67; HISTONE DEACETYLASE 1; MESSENGER RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DLX; TRANSCRIPTION FACTOR PITX2; UNCLASSIFIED DRUG; ENTINOSTAT;

5' UNTRANSLATED REGION; ARTICLE; CELL STRAIN; CELL STRAIN NT2; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DNA FLANKING REGION; DNA METHYLATION; ENZYME INHIBITION; EXON; GAD1 GENE; GENE; GENE CONTROL; GENE DELETION; GENE SEQUENCE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NEURAL STEM CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY SEQUENCE; TRANSCRIPTION INITIATION SITE; ANIMAL TISSUE; CHROMATIN IMMUNOPRECIPITATION; DRUG ACTIVITY; DRUG POTENCY; ENZYME ACTIVATION; GAD67 GENE; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; INTERNEURON; MOUSE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; REPORTER GENE; SINGLE NUCLEOTIDE POLYMORPHISM;

5' UNTRANSLATED REGIONS; BASE SEQUENCE; BENZAMIDES; CELL CULTURE TECHNIQUES; CPG ISLANDS; DNA; DNA METHYLATION; GENES, REPORTER; GENETIC VECTORS; GLUTAMATE DECARBOXYLASE; HISTONE DEACETYLASE INHIBITORS; HUMANS; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; PYRIDINES; SEQUENCE DELETION; TRANS-ACTIVATORS; TRANSFECTION; UNTRANSLATED REGIONS;

EID: 79954601665     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2010.09.017     Document Type: Article

References (56)

1. S. Akbarian, and H.-S. Huang Molecular and cellular mechanisms of altered GAD1/GAD67 expression in schizophrenia and related disorders Brain Res. Rev. 52 2006 293 304 (Pubitemid 44291805)
2. S. Akbarian, J.J. Kim, S.G. Potkin, J.O. Hagman, A. Tafazzoli, W.E. Bunney, 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. B.A. Amendt, L.B. Sutherland, and A.F. Russo Multifunctional role of the Pitx2 homeodomain protein C-terminal tail Mol. Cell. Biol. 19 1999 7001 7010 (Pubitemid 29441882)
4. S.A. Anderson, D.D. Eisenstat, L. Shi, and J.L.R. Rubenstein Differential origins of neocortical projection and local circuit neurons: role of Dlx genes in neocortical interneuronogensis Cereb. Cortex 9 1999 646 654 (Pubitemid 29441506)
5. H. Asada, Y. Kawamura, K. Maruyama, H. Kume, R. Ding, F.Y. Ji, N. Kanbara, H. Kuzume, M. Sanbo, T. Yagi, and K. Obata Cleft palate and decreased brain gamma-aminobutyric acid in mice lacking the 67- kDa isoform of glutamic acid decarboxylase Proc. Natl. Acad. Sci. U S A 94 1997 6496 6499 (Pubitemid 27270713)
6. S.J. Bray, W.A. Johnson, J. Hirsh, U. Heberlein, and R. Tjian A cis-acting element and associated binding factor required for CNS expression of the Drosophila melanogaster dopa decarboxylase gene EMBO J. 1988 177 188
7. D.-F. Bu, and A.J. Tobin The exon-intron organization of the genes (GAD1 and GAD2) encoding two human glutamate decarboxylases (GAD67 and GAD65) suggests that they derive from a common ancestral GAD Genomics 21 1994 222 228 (Pubitemid 24157747)
8. G. Buschhausen, B. Wittig, M. Graessmann, and A. Graessmann Chromatin structure is required to block transcription of the methylated herpes simplex virus thymidine kinase gene Proc. Natl. Acad. Sci. U S A 84 1987 1177 1181 (Pubitemid 17027315)
9. B. Chattopadhyaya, G. Di Cristo, C.Z. Wu, G. Knott, S. Kuhlman, Y. Fu, R.D. Palmiter, and Z.J. Huang GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex Neuron 54 2007 889 903 (Pubitemid 46907499)
10. Y. Chen, R.P. Sharma, R.H. Costa, E. Costa, and D.R. Grayson On the epigenetic regulation of the human reelin promoter Nucleic Acids Res. 30 2002 2930 2939 (Pubitemid 34778154)
11. 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. 103 2007 65 655
12. S.D. Chessler, and A. Lernmark Alternative splicing of GAD67 results in the synthesis of a third form of glutamic-acid decarboxylase in human islets and other non-neural tissues J. Biol. Chem. 275 2000 5188 5192 (Pubitemid 30108922)
13. B.G. Condie, G. Gain, D.I. Gottlieb, and M.R. Capecchi Cleft palate in mice with a targeted mutation in the γ-aminobutyric acid-producing enzyme glutamic acid decarboxylase 67 Proc. Natl. Acad. Sci. U S A 94 1997 11451 11455 (Pubitemid 27451019)
14. N. Detich, V. Bovenzi, and M. Szyf Valproate induces replication- independent active DNA demethylation J. Biol. Chem. 278 2003 27586 27592 (Pubitemid 36899944)
15. E. Dong, R.C. Agis-Balboa, M.V. Simonini, D.R. Grayson, E. Costa, and A. Guidotti 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 (Pubitemid 41266401)
16. E. Dong, A. Guidotti, D.R. Grayson, and E. Costa Demethylation of reelin and glutamic acid decarboxylase 67 brain promoters is induced by hyperacetylation of histones Proc. Natl. Acad. Sci. U S A 104 2007 4676 4681 (Pubitemid 47186284)
17. M.G. Erlander, and A.J. Tobin A transcriptional regulatory element of the gene encoding the 67,000-Mr form of human glutamate decarboxylase is similar to a Drosophila regulatory element J. Neurochem. 58 1992 2182 2190
18. G. Gonzalez-Burgos, T. Hashimoto, and D.A. Lewis Alterations of cortical GABA neurons and network oscillations in schizophrenia Curr. Psychiatry Rep. 12 2010 335 344
19. 67) expression in schizophrenia and bipolar disorder: a postmortem brain study Arch. Gen. Psych. 57 2000 1061 1069
20. A. Guidotti, J. Auta, J.M. Davis, E. Dong, D.R. Grayson, M. Veldic, X. Zhang, and E. Costa GABAergic dysfunction in schizophrenia: a new treatment on the horizon Psychopharmacology 180 2005 191 205 (Pubitemid 40909664)
21. 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
22. S. Heckers, D. Stone, J. Walsh, J. Schick, P. Koul, and F.M. Benes Differential hippocampal expression of glutamic acid decarboxylase 65 and 67 messenger RNA in bipolar disorder and schizophrenia Arch. Gen. Psychiatry 59 2002 521 529 (Pubitemid 34602934)
23. H.-S. Huang, and S. Akbarian GAD1 mRNA expression and DNA methylation in prefrontal cortex of subjects with schizophrenia PloS ONE 2 2007 e809
24. H.-S. Huang, A. Matevossian, C. Whittle, S.Y. Kim, A. Schumacher, S.O. 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)
25. R.S. Illingworth, and A.P. Bird CpG islands-a rough guide FEBS Lett. 583 2009 1713 1720
26. S.W. Jeong, and A. Stein Micrococcal nuclease digestion of nculei reveals extended nucleosome ladders having anomolous DNA lengths for chromatin assembled on non-replicating plasmids in transfected cells Nuc. Acids Res. 22 1994 370 375 (Pubitemid 24160857)
27. K. Kanno, Y. Suzuki, A. Yamada, Y. Aoki, S. Kure, and Y. Matsubara Association between nonsyndromic cleft lip with or without cleft palate and the glutamate decarboxylase 67 gene in the Japanese population Am. J. Med. Genet. 127A 2004 11 16 (Pubitemid 38937199)
28. S.F. Kash, R.S. Johnson, L.H. Tecott, J.L. Noebels, R.D. Mayfield, D. Hanahan, and S. Baekkeskov Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase Proc. Natl. Acad. Sci. USA 94 1997 14060 14065 (Pubitemid 28009709)
29. S. Kim, and M.J. Webster The Stanley Neuropathology Consortium integrative database: a novel, web-based tool for exploring neuropathological markers in psychiatric disorders and the biological processes associated with abnormalities of those markers Neuropsychopharmacology 35 2010 473 482
30. M. Klug, and M. Rehli Functional analysis of promoter CpG methylation using a CpG-free luciferase reporter vector Epigenetics 1 2006 127 130
31. M. Kundakovic, Y. Chen, E. Costa, and D.R. Grayson DNA methyltransferase inhibitors coordinately induce expression of the human reelin and glutamic acid decarboxylase genes Mol. Pharmacol. 71 2007 644 653 (Pubitemid 46294076)
32. M. Kundakovic, Y. Chen, A. Guidotti, and D.R. Grayson The reelin and GAD67 promoters are activated by epigenetic drugs that facilitate the disruption of local repressor complexes Mol. Pharmacol. 75 2009 342 354
33. C. Ladd-Acosta, J. Pevsner, S. Sabunciyan, R.H. Yolken, M.J. Webster, T. Dinkins, P.A. Callinan, J.-B. Fan, J.B. Potash, and A.P. Feinberg DNA methylation signatures within the human brain Am. J. Hum. Genet. 81 2007 1304 1315 (Pubitemid 350211460)
34. M.D. Lundorf, H.N. Buttenshon, L. Foldager, D.H.R. Blackwood, W.J. Muir, V. Murray, A.J. Pelosi, T.A. Kruse, H. Ewald, and O. Mors Mutational screening and association study of glutamate decarboxylase I as a candidate susceptibility gene for bipolar affective disorder and schizophrenia Am. J. Med. Genet. 135B 2004 94 101
35. S. Marenco, A.A. Savostyanova, J.W. van der Veen, M. Geramita, A. Stern, A.S. Barnett, B. Kolachana, E. Radulescu, F. Zhang, J.H. Callicott, R.E. Straub, J. Shen, and D.R. Weinberger Genetic modulation of GABA levels in the anterior cingulate cortex by GAD1 and COMT Neuropsychopharmacol 35 2010 1708 1717
36. 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)
37. J.S. Noh, R.P. Sharma, M. Veldic, A.A. Salvacion, X. Jia, Y. Chen, E. Costa, A. Guidotti, and D.R. Grayson DNA methyltransferase 1 regulates reelin mRNA expression in primary mouse cortical cultures Proc. Natl. Acad. Sci. U S A 102 2005 1749 1754 (Pubitemid 40209239)
38. R. Poirier, H. Cheval, C. Mailhes, S. Garel, P. Charnay, S. Davis, and S. Laroche Distinct functions of Egr gene family members in cognitive processes Front. Neurosci. 2 2008 47 55
39. E.V. Semina, R. Reiter, N.J. Leysens, L.M. Alward, K.W. Small, N.A. Datson, J. Siegel-Bartelt, D. Bierke-Nelson, P. Bitoun, B.U. Zabel, J.C. Carey, and J.C. Murray Cloning and characterization of a novel bicoid-related homeobox transcription factor gene, RIEG, involved in Rieger syndrome Nat. Genet. 14 1996 392 399 (Pubitemid 26414582)
40. R.P. Sharma, D.P. Gavin, and D.R. Grayson CpG methylation in neurons: message, memory, or mask? Neuropsychopharmacol 2010 epub ahead of print
41. K.D. Siegmund, C.M. Connor, M. Campan, T.I. Long, D.J. Weisenberger, D. Biniszkiewicz, R. Jaenisch, P.W. Laird, and S. Akbarian DNA methylation in the human cerebral cortex is dynamically regulated throughout the life span and involves differentiated neurons PloS ONE 9 2007 e895
42. R.E. Straub, B.K. Lipska, M.F. Egan, T.E. Goldberg, J.H. Callicott, M.B. Mayhew, R.K. Vakkalanka, B.S. Kolachana, J.E. Kleinman, and D.R. Weinberger Allelic variation in GAD1 (GAD67) is associated with schizophrenia and influences cortical function and gene expression Mol. Psychiatry 12 2007 854 869 (Pubitemid 47347790)
43. T. Stühmer, S.A. Anderson, M. Ekker, and J.L.R. Rubenstein Ectopic expression of the Dlx genes induces glutamic acid decarboxylase and Dlx expression Development 129 2002 245 252 (Pubitemid 34863792)
44. T. Stühmer, L. Puelles, M. Ekker, and J.L.R. Rubenstein Expression from a Dlx gene enhancer marks adult mouse cortical GABAergic neurons Cereb. Cortex 12 2002 75 85 (Pubitemid 33152019)
45. G. Szabo, Z. Katarova, E. Kortvely, R.J. Greenspan, and Z. Urban Structure of the mouse gene encoding the 67-kD form of glutamic acid decarboxylase DNA Cell Biol. 15 1996 1081 1091 (Pubitemid 27014161)
46. M. Thompson, C.S. Weickert, E. Wyatt, and M.J. Webster Decreased glutamic acid decarboxylase67 mRNA expression in multiple brain areas of patients with schizophrenia and mood disorders J. Psych. Res. 43 2009 970 977
47. E.F. Torrey, B.M. Barci, M.J. Webster, J.J. Bartko, J.H. Meader-Woodruff, and M.B. Knable Neurochemical markers for schizophrenia, bipolar disorder, and major depression in post-mortem brains Biol. Psychiatry 57 2005 252 260 (Pubitemid 40187369)
48. 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)
49. L. Tremolizzo, M.S. Doueiri, E. Dong, D.R. Grayson, 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)
50. M. Veldic, H.M. Caruncho, W.S. Liu, J. Davis, R. Satta, D.R. Grayson, A. Guidotti, and E. Costa 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 (Pubitemid 38084253)
51. M. Veldic, A. Guidotti, E. Maloku, J.M. Davis, and E. Costa In psychosis, cortical interneurons overexpress DNA-methyltransferase I Proc. Natl. Acad. Sci. U S A 102 2005 2152 2157 (Pubitemid 40262027)
52. J.J. Westmoreland, J. McEwen, B.A. Moore, Y. Jin, and B.G. Condie Conserved function of Caenorhabditis elegans UNC-30 and mouse Pitx2 in controlling GABAergic neuron differentiation J. Neurosci. 21 2001 6810 6819 (Pubitemid 32781124)
53. Y. Yanagawa, T. Kobayahi, T. Kamei, K. Ishii, M. Nishijima, A. Takaku, T. Kobayashi, and S. Tamura Structure and alternative promoters of the mouse glutamic acid decarboxylase gene Biochem. J. 326 1997 573 578 (Pubitemid 27417239)
54. T.-Y. Zhang, and M.J. Meaney Epigenetics and the environmental regulation of the genome and its function Annu. Rev. Psychol. 61 2010 439 466
55. D. Zhang, L. Cheng, J.A. Badner, C. Chen, Q. Chen, W. Luo, D.W. Craig, M. Redman, E.S. Gershon, and C. Liu Genetic control of individual differences in gene-specific methylation in human brain Am. J. Hum. Genet. 86 2010 411 419
56. Zhang, T.-Y., Hellstrom, I.C., Bagot, R.C., Wen, X., Diorio, J., Meaney, M.J., Maternal care and DNA methylation of a glutamic acid decarboxylase 1 promoter in rat hippocampus. J. Neurosci. Manuscript in press.