The site specific demethylation in the 5′-regulatory area of NMDA receptor 2B subunit gene associated with CIE-induced up-regulation of transcription

PLoS ONE

Volumn 5, Issue 1, 2010, Pages

  Qiang, Mei ^a   Denny, Ashley ^a   Chen, Jiguo ^c   Ticku, Maharaj K ^a   Yan, Bo ^b   Henderson, George ^d  

^a Mays Cancer Center at UT Health San Antonio   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c MISSISSIPPI STATE UNIVERSITY   (United States)

^d TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; BISULFITE; CRE RECOMBINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; DNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PRIMER DNA;

ANIMAL CELL; ARTICLE; BRAIN CELL; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; DEMETHYLATION; DNA METHYLATION; EPIGENETICS; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SEQUENCE; IN VITRO STUDY; MOUSE; NONHUMAN; PROMOTER REGION; PYROSEQUENCING; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; DRUG EFFECT; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; REGULATORY SEQUENCE;

ANIMALS; BASE SEQUENCE; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; CPG ISLANDS; DNA METHYLATION; DNA PRIMERS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EPIGENESIS, GENETIC; ETHANOL; MICE; MICE, INBRED C57BL; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; RECEPTORS, N-METHYL-D-ASPARTATE; REGULATORY SEQUENCES, NUCLEIC ACID; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 77649286162     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008798     Document Type: Article

References (76)

1. Cagetti E, Liang J, Spigelman I, Olsen RW (2003) Withdrawal from chronic intermittent ethanol treatment changes subunit composition, reduces synaptic function, and decreases behavioral responses to positive allosteric modulators of GABAA receptors. Mol Pharmacol 63: 53-64.
2. Kokka N, Sapp DW, Taylor AM, Olsen RW (1993) The kindling model of alcohol dependence: similar persistent reduction in seizure threshold to pentylenetetrazol in animals receiving chronic ethanol or chronic pentylenetetrazol. Alcohol Clin Exp Res 17: 525-531.
3. Nestler EJ (2001) Molecular basis of long-term plasticity underlying addiction. Nat Rev Neurosci 2: 119-128.
4. Ron D, Jurd R (2005) The "ups and downs" of signaling cascades in addiction. Sci STKE 2005: re14.
5. Nieuwenhuys R (1994) The neocortex. An overview of its evolutionary development, structural organization and synaptology. Anat Embryol (Berl) 190: 307-337.
6. Javitt DC (2004) Glutamate as a therapeutic target in psychiatric disorders. Mol Psychiatry 9: 984-997, 979.
7. Trevisan L, Fitzgerald LW, Brose N, Gasic GP, Heinemann SF, et al. (1994) Chronic ingestion of ethanol up-regulates NMDAR1 receptor subunit immunoreactivity in rat hippocampus. J Neurochem 62: 1635-1638.
8. Follesa P, Ticku MK (1995) Chronic ethanol treatment differentially regulates NMDA receptor subunit mRNA expression in rat brain. Brain Res Mol Brain Res 29: 99-106.
9. Carpenter-Hyland EP, Woodward JJ, Chandler LJ (2004) Chronic ethanol induces synaptic but not extrasynaptic targeting of NMDA receptors. J Neurosci 24: 7859-7868.
10. Nagy J, Laszlo L (2002) Increased sensitivity to NMDA is involved in alcohol-withdrawal induced cytotoxicity observed in primary cultures of cortical neurones chronically pre-treated with ethanol. Neurochem Int 40: 585-591.
11. Ronald KM, Mirshahi T, Woodward JJ (2001) Ethanol inhibition of N-methyl-D-aspartate receptors is reduced by site-directed mutagenesis of a transmembrane domain phenylalanine residue. J Biol Chem 276: 44729-44735.
12. Ogata J, Shiraishi M, Namba T, Smothers CT, Woodward JJ, et al. (2006) Effects of anesthetics on mutant N-methyl-D-aspartate receptors expressed in Xenopus oocytes. J Pharmacol Exp Ther 318: 434-443.
13. Nagy J, Horvath C, Farkas S, Kolok S, Szombathelyi Z (2004) NR2B subunit selective NMDA antagonists inhibit neurotoxic effect of alcohol-withdrawal in primary cultures of rat cortical neurones. Neurochem Int 44: 17-23.
14. Narita M, Soma M, Mizoguchi H, Tseng LF, Suzuki T (2000) Implications of the NR2B subunit-containing NMDA receptor localized in mouse limbic forebrain in ethanol dependence. Eur J Pharmacol 401: 191-195.
15. Sheela Rani CS, Ticku MK (2006) Comparison of chronic ethanol and chronic intermittent ethanol treatments on the expression of GABA(A) and NMDA receptor subunits. Alcohol 38: 89-97.
16. Qiang M, Denny AD, Ticku MK (2007) Chronic Intermittent Ethanol Treatment Selectively Alters NMDA Receptor Subunits Surface Expression in Cultured Cortical Neurons. Mol Pharmacol.
17. Nelson TE, Ur CL, Gruol DL (2005) Chronic intermittent ethanol exposure enhances NMDA-receptor-mediated synaptic responses and NMDA receptor expression in hippocampal CA1 region. Brain Res 1048: 69-79.
18. Jiang Y, Langley B, Lubin FD, Renthal W, Wood MA, et al. (2008) Epigenetics in the nervous system. J Neurosci 28: 11753-11759.
19. Mattson MP (2003) Methylation and acetylation in nervous system development and neurodegenerative disorders. Ageing Res Rev 2: 329-342.
20. Marutha Ravindran CR, Ticku MK (2004) Changes in methylation pattern of NMDA receptor NR2B gene in cortical neurons after chronic ethanol treatment in mice. Brain Res Mol Brain Res 121: 19-27.
21. Colvis CM, Pollock JD, Goodman RH, Impey S, Dunn J, et al. (2005) Epigenetic mechanisms and gene networks in the nervous system. J Neurosci 25: 10379-10389.
22. Levenson JM, Sweatt JD (2006) Epigenetic mechanisms: a common theme in vertebrate and invertebrate memory formation. Cell Mol Life Sci 63: 1009-1016.
23. Nelson ED, Kavalali ET, Monteggia LM (2008) Activity-dependent suppression of miniature neurotransmission through the regulation of DNA methylation. J Neurosci 28: 395-406.
24. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, et al. (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7: 847-854.
25. Roth TL, Sweatt JD (2009) Regulation of chromatin structure in memory formation. Curr Opin Neurobiol 19: 336-342.
26. Levenson JM, Sweatt JD (2005) Epigenetic mechanisms in memory formation. Nat Rev Neurosci 6: 108-118.
27. Veldic M, Kadriu B, Maloku E, Agis-Balboa RC, Guidotti A, et al. (2007) Epigenetic mechanisms expressed in basal ganglia GABAergic neurons differentiate schizophrenia from bipolar disorder. Schizophr Res 91: 51-61.
28. Ruzicka WB, Zhubi A, Veldic M, Grayson DR, Costa E, et al. (2007) Selective epigenetic alteration of layer I GABAergic neurons isolated from prefrontal cortex of schizophrenia patients using laser-assisted microdissection. Mol Psychiatry 12: 385-397.
29. Ma DK, Jang MH, Guo JU, Kitabatake Y, Chang ML, et al. (2009) Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323: 1074-1077.
30. Wu H, Sun YE (2009) Reversing DNA methylation: new insights from neuronal activity-induced Gadd45b in adult neurogenesis. Sci Signal 2: pe17.
31. Lubin FD, Roth TL, Sweatt JD (2008) Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J Neurosci 28: 10576-10586.
32. Dupont JM, Tost J, Jammes H, Gut IG (2004) De novo quantitative bisulfite sequencing using the pyrosequencing technology. Anal Biochem 333: 119-127.
33. Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, et al. (1998) Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 19: 187-191.
34. Nan X, Campoy FJ, Bird A (1997) MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell 88: 471-481.
35. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, et al. (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393: 386-389.
36. Hendrich B, Bird A (1998) Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 18: 6538-6547.
37. Qiang M, Ticku MK (2005) Role of AP-1 in ethanol-induced N-methyl-Daspartate receptor 2B subunit gene up-regulation in mouse cortical neurons. J Neurochem 95: 1332-1341.
38. Rani CS, Qiang M, Ticku MK (2005) Potential role of cAMP response element-binding protein in ethanol-induced N-methyl-D-aspartate receptor 2B subunit gene transcription in fetal mouse cortical cells. Mol Pharmacol 67: 2126-2136.
39. Leonhardt H, Page AW, Weier HU, Bestor TH (1992) A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell 71: 865-873.
40. Inano K, Suetake I, Ueda T, Miyake Y, Nakamura M, et al. (2000) Maintenance-type DNA methyltransferase is highly expressed in post-mitotic neurons and localized in the cytoplasmic compartment. J Biochem 128: 315-321.
41. Noh JS, Sharma RP, Veldic M, Salvacion AA, Jia X, et al. (2005) DNA methyltransferase 1 regulates reelin mRNA expression in mouse primary cortical cultures. Proc Natl Acad Sci U S A 102: 1749-1754.
42. Veldic M, Caruncho HJ, Liu WS, Davis J, Satta R, et al. (2004) DNA-methyltransferase 1 mRNA is selectively overexpressed in telencephalic GABAergic interneurons of schizophrenia brains. Proc Natl Acad Sci U S A 101: 348-353.
43. Pandey SC, Ugale R, Zhang H, Tang L, Prakash A (2008) Brain chromatin remodeling: a novel mechanism of alcoholism. J Neurosci 28: 3729-3737.
44. Krystal JH, Petrakis IL, Mason G, Trevisan L, D'Souza DC (2003) N-methyl-Daspartate glutamate receptors and alcoholism: reward, dependence, treatment, and vulnerability. Pharmacol Ther 99: 79-94.
45. Miller CA, Sweatt JD (2007) Covalent modification of DNA regulates memory formation. Neuron 53: 857-869.
46. Bhattacharya SK, Ramchandani S, Cervoni N, Szyf M (1999) A mammalian protein with specific demethylase activity for mCpG DNA. Nature 397: 579-583.
47. Jair KW, Bachman KE, Suzuki H, Ting AH, Rhee I, et al. (2006) De novo CpG island methylation in human cancer cells. Cancer Res 66: 682-692.
48. Martinowich K, Hattori D, Wu H, Fouse S, He F, et al. (2003) DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 302: 890-893.
49. Satta R, Maloku E, Zhubi A, Pibiri F, Hajos M, et al. (2008) Nicotine decreases DNA methyltransferase 1 expression and glutamic acid decarboxylase 67 promoter methylation in GABAergic interneurons. Proc Natl Acad Sci U S A 105: 16356-16361.
50. Leu YW, Rahmatpanah F, Shi H, Wei SH, Liu JC, et al. (2003) Double RNA interference of DNMT3b and DNMT1 enhances DNA demethylation and gene reactivation. Cancer Res 63: 6110-6115.
51. Kangaspeska S, Stride B, Metivier R, Polycarpou-Schwarz M, Ibberson D, et al. (2008) Transient cyclical methylation of promoter DNA. Nature 452: 112-115.
52. Szyf M (2005) DNA methylation and demethylation as targets for anticancer therapy. Biochemistry (Mosc) 70: 533-549.
53. Endres M, Meisel A, Biniszkiewicz D, Namura S, Prass K, et al. (2000) DNA methyltransferase contributes to delayed ischemic brain injury. J Neurosci 20: 3175-3181.
54. Tremolizzo L, Carboni G, Ruzicka WB, Mitchell CP, Sugaya I, et al. (2002) An epigenetic mouse model for molecular and behavioral neuropathologies related to schizophrenia vulnerability. Proc Natl Acad Sci U S A 99: 17095-17100.
55. Santi DV, Norment A, Garrett CE (1984) Covalent bond formation between a DNA-cytosine methyltransferase and DNA containing 5-azacytosine. Proc Natl Acad Sci U S A 81: 6993-6997.
56. Creusot F, Acs G, Christman JK (1982) Inhibition of DNA methyltransferase and induction of Friend erythroleukemia cell differentiation by 5-azacytidine and 5-aza-2′-deoxycytidine. J Biol Chem 257: 2041-2048.
57. Gius D, Cui H, Bradbury CM, Cook J, Smart DK, et al. (2004) Distinct effects on gene expression of chemical and genetic manipulation of the cancer epigenome revealed by a multimodality approach. Cancer Cell 6: 361-371.
58. Ghoshal K, Datta J, Majumder S, Bai S, Kutay H, et al. (2005) 5-Aza-deoxycytidine induces selective degradation of DNA methyltransferase 1 by a proteasomal pathway that requires the KEN box, bromo-adjacent homology domain, and nuclear localization signal. Mol Cell Biol 25: 4727-4741.
59. Pascale RM, Simile MM, Satta G, Seddaiu MA, Daino L, et al. (1991) Comparative effects of L-methionine, S-adenosyl-L-methionine and 5′-methylthioadenosine on the growth of preneoplastic lesions and DNA methylation in rat liver during the early stages of hepatocarcinogenesis. Anticancer Res 11: 1617-1624.
60. Szyf M, Pakneshan P, Rabbani SA (2004) DNA methylation and breast cancer. Biochem Pharmacol 68: 1187-1197.
61. Cedar H (1988) DNA methylation and gene activity. Cell 53: 3-4.
62. Jenuwein T, Forrester WC, Fernandez-Herrero LA, Laible G, Dull M, et al. (1997) Extension of chromatin accessibility by nuclear matrix attachment regions. Nature 385: 269-272.
63. Keshet I, Yisraeli J, Cedar H (1985) Effect of regional DNA methylation on gene expression. Proc Natl Acad Sci U S A 82: 2560-2564.
64. Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33 Suppl: 245-254.
65. Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447: 407-412.
66. Ng HH, Bird A (1999) DNA methylation and chromatin modification. Curr Opin Genet Dev 9: 158-163.
67. Wu LP, Wang X, Li L, Zhao Y, Lu S, et al. (2008) Histone deacetylase inhibitor depsipeptide activates silenced genes through decreasing both CpG and H3K9 methylation on the promoter. Mol Cell Biol 28: 3219-3235.
68. Vaissiere T, Sawan C, Herceg Z (2008) Epigenetic interplay between histone modifications and DNA methylation in gene silencing. Mutat Res 659: 40-48.
69. Chang Q, Khare G, Dani V, Nelson S, Jaenisch R (2006) The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression. Neuron 49: 341-348.
70. Chao HT, Zoghbi HY, Rosenmund C (2007) MeCP2 controls excitatory synaptic strength by regulating glutamatergic synapse number. Neuron 56: 58-65.
71. Chahrour M, Jung SY, Shaw C, Zhou X, Wong ST, et al. (2008) MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320: 1224-1229.
72. Ramchandani S, Bhattacharya SK, Cervoni N, Szyf M (1999) DNA methylation is a reversible biological signal. Proc Natl Acad Sci U S A 96: 6107-6112.
73. Meaney MJ, Szyf M (2005) Maternal care as a model for experience-dependent chromatin plasticity? Trends Neurosci 28: 456-463.
74. Qiang M, Rani CS, Ticku MK (2005) Neuron-restrictive silencer factor regulates the N-methyl-D-aspartate receptor 2B subunit gene in basal and ethanol-induced gene expression in fetal cortical neurons. Mol Pharmacol 67: 2115-2125.
75. Brakensiek K, Wingen LU, Langer F, Kreipe H, Lehmann U (2007) Quantitative high-resolution CpG island mapping with Pyrosequencing reveals disease-specific methylation patterns of the CDKN2B gene in myelodysplastic syndrome and myeloid leukemia. Clin Chem 53: 17-23.
76. Robertson KD, Hayward SD, Ling PD, Samid D, Ambinder RF (1995) Transcriptional activation of the Epstein-Barr virus latency C promoter after 5-azacytidine treatment: evidence that demethylation at a single CpG site is crucial. Mol Cell Biol 15: 6150-6159.