Gadd45b and N-methyl-d-aspartate induced DNA demethylation in postmitotic neurons

Epigenomics

Volumn 7, Issue 4, 2015, Pages 567-579

  Gavin, David P ^a,b   Kusumo, Handojo ^a,b   Sharma, Rajiv P ^a,b   Guizzetti, Marina ^a,b,c   Guidotti, Alessandro ^b   Pandey, Subhash C ^a,b  

^a JESSE BROWN VA MEDICAL CENTER   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c PORTLAND VA MEDICAL CENTER   (United States)

Author keywords

alcoholism; CpG; epigenetic; histone; schizophrenia

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; 5 METHYLCYTOSINE; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 1; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR IXA; COMPLEMENTARY DNA; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45B; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; AMINO ACID RECEPTOR STIMULATING AGENT; CELL CYCLE PROTEIN; GADD45A PROTEIN, MOUSE; N METHYLASPARTIC ACID; NUCLEAR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL CULTURE; CONTROLLED STUDY; DEMETHYLATION; DENTATE GYRUS; DNA METHYLATION; EXCISION REPAIR; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VITRO STUDY; MENTAL DISEASE; MOUSE; NEURAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; BRAIN CORTEX; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; PYRAMIDAL NERVE CELL;

5-METHYLCYTOSINE; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL CYCLE PROTEINS; CELLS, CULTURED; CEREBRAL CORTEX; DNA METHYLATION; EXCITATORY AMINO ACID AGONISTS; MICE; N-METHYLASPARTATE; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; PYRAMIDAL CELLS;

EID: 84933525272     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.15.12     Document Type: Article

References (63)

1. Weaver IC, Cervoni N, Champagne FA et al. Epigenetic programming by maternal behavior. Nat. Neurosci. 7(8), 847-854 (2004).
2. Sharma RP, Gavin DP, Grayson DR. CpG methylation in neurons: message, memory, or mask? Neuropsychopharmacology 35(10), 2009-2020 (2010).
3. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 16(1), 6-21 (2002).
4. Cortese R, Lewin J, Backdahl L et al. Genome-wide screen for differential DNA methylation associated with neural cell differentiation in mouse. PLoS ONE 6(10), e26002 (2011).
5. De Carvalho DD, You JS, Jones PA. DNA methylation and cellular reprogramming. Trends Cell Biol. 20(10), 609-617 (2010).
6. Deaton AM, Webb S, Kerr AR et al. Cell type-specific DNA methylation at intragenic CpG islands in the immune system. Genome Res. 21(7), 1074-1086 (2011).
7. Iwamoto K, Bundo M, Ueda J et al. Neurons show distinctive DNA methylation profile and higher interindividual variations compared with non-neurons. Genome Res. 21(5), 688-696 (2011).
8. Levenson JM, Roth TL, Lubin FD et al. Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. J. Biol. Chem. 281(23), 15763-15773 (2006).
9. Mill J, Petronis A. Profiling DNA methylation from small amounts of genomic DNA starting material: efficient sodium bisulfite conversion and subsequent whole-genome amplification. Methods Mol. Biol. 507, 371-381 (2009).
10. Abdolmaleky HM, Cheng KH, Faraone SV et al. Hypomethylation of MB-COMT promoter is a major risk factor for schizophrenia and bipolar disorder. Hum. Mol. Genet. 15(21), 3132-3145 (2006).
11. Abdolmaleky HM, Cheng KH, Russo A et al. Hypermethylation of the reelin (RELN) promoter in the brain of schizophrenic patients: a preliminary report. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 134B(1), 60-66 (2005).
12. Guidotti A, Auta J, Chen Y et al. Epigenetic GABAergic targets in schizophrenia and bipolar disorder. Neuropharmacology 60(7-8), 1007-1016 (2011).
13. Feng J, Chang H, Li E, Fan G. Dynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system. J. Neurosci. Res. 79(6), 734-746 (2005).
14. Feng J, Zhou Y, Campbell SL et al. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat. Neurosci. 13(4), 423-430 (2010).
15. Guo JU, Su Y, Zhong C, Ming GL, Song H. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145(3), 423-434 (2011).
16. Ito S, D'Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466(7310), 1129-1133 (2010).
17. Pastor WA, Pape UJ, Huang Y et al. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 473(7347), 394-397 (2011).
18. Wu H, D'Alessio AC, Ito S et al. Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature 473(7347), 389-393 (2011).
19. Xu Y, Wu F, Tan L et al. Genome-wide regulation of 5hmC, 5mC, and gene expression by Tet1 hydroxylase in mouse embryonic stem cells. Mol. Cell 42(4), 451-464 (2011).
20. Ficz G, Branco MR, Seisenberger S et al. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 473(7347), 398-402 (2011).
21. Koh KP, Yabuuchi A, Rao S et al. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell. Stem Cell. 8(2), 200-213 (2011).
22. Williams K, Christensen J, Pedersen MT et al. TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 473(7347), 343-348 (2011).
23. Kaas GA, Zhong C, Eason DE et al. TET1 controls CNS 5-methylcytosine hydroxylation, active DNA demethylation, gene transcription, and memory formation. Neuron 79(6), 1086-1093 (2013).
24. Morgan HD, Dean W, Coker HA, Reik W, Petersen-Mahrt SK. Activation-induced cytidine deaminase deaminates 5-methylcytosine in DNA and is expressed in pluripotent tissues: implications for epigenetic reprogramming. J. Biol. Chem. 279(50), 52353-52360 (2004).
25. Popp C, Dean W, Feng S et al. Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463(7284), 1101-1105 (2010).
26. Hendrich B, Hardeland U, Ng HH, Jiricny J, Bird A. The thymine glycosylase MBD4 can bind to the product of deamination at methylated CpG sites. Nature 401(6750), 301-304 (1999).
27. He YF, Li BZ, Li Z et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333(6047), 1303-1307 (2011).
28. Cortellino S, Xu J, Sannai M et al. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146(1), 67-79 (2011).
29. Rai K, Huggins IJ, James SR, Karpf AR, Jones DA, Cairns BR. DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and Gadd45. Cell 135(7), 1201-1212 (2008).
30. Spruijt CG, Gnerlich F, Smits AH et al. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 152(5), 1146-1159 (2013).
31. Kemmerich K, Dingler FA, Rada C, Neuberger MS. 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 Res. 40(13), 6016-6025 (2012).
32. Hevroni D, Rattner A, Bundman M et al. Hippocampal plasticity involves extensive gene induction and multiple cellular mechanisms. J. Mol. Neurosci. 10(2), 75-98 (1998).
33. Keeley MB, Wood MA, Isiegas C et al. Differential transcriptional response to nonassociative and associative components of classical fear conditioning in the amygdala and hippocampus. Learn. Mem. 13(2), 135-142 (2006).
34. Leach PT, Poplawski SG, Kenney JW et al. Gadd45b knockout mice exhibit selective deficits in hippocampus-dependent longterm memory. Learn. Mem. 19(8), 319-324 (2012).
35. Sultan FA, Wang J, Tront J, Liebermann DA, Sweatt JD. Genetic deletion of Gadd45b, a regulator of active DNA demethylation, enhances long-term memory and synaptic plasticity. J. Neurosci. 32, 17059-17066 (2012).
36. Ma DK, Jang MH, Guo JU et al. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323(5917), 1074-1077 (2009).
37. Yi YW, Kim D, Jung N, Hong SS, Lee HS, Bae I. Gadd45 family proteins are coactivators of nuclear hormone receptors. Biochem. Biophys. Res. Commun. 272(1), 193-198 (2000).
38. Carrier F, Georgel PT, Pourquier P et al. Gadd45, a p53-responsive stress protein, modifies DNA accessibility on damaged chromatin. Mol. Cell. Biol. 19(3), 1673-1685 (1999).
39. Greenberg ME, Xu B, Lu B, Hempstead BL. New insights in the biology of BDNF synthesis and release: implications in CNS function. J. Neurosci. 29(41), 12764-12767 (2009).
40. Zuccato C, Cattaneo E. Brain-derived neurotrophic factor in neurodegenerative diseases. Nat. Rev. Neurol. 5(6), 311-322 (2009).
41. Aid T, Kazantseva A, Piirsoo M, Palm K, Timmusk T. Mouse and rat BDNF gene structure and expression revisited. J. Neurosci. Res. 85(3), 525-535 (2007).
42. Chen WG, Chang Q, Lin Y et al. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 302(5646), 885-889 (2003).
43. Martinowich K, Hattori D, Wu H et al. DNA methylationrelated chromatin remodeling in activity-dependent BDNF gene regulation. Science 302(5646), 890-893 (2003).
44. Sales AJ, Biojone C, Terceti MS, Guimaraes FS, Gomes MV, Joca SR. Antidepressant-like effect induced by systemic and intra-hippocampal administration of DNA methylation inhibitors. Br. J. Pharmacol. 164(6), 1711-1721 (2011).
45. Gavin DP, Chase KA, Sharma RP. Active DNA demethylation in post-mitotic neurons: A reason for optimism. Neuropharmacology 75, 233-245 (2013).
46. Ikegame T, Bundo M, Sunaga F et al. DNA methylation analysis of BDNF gene promoters in peripheral blood cells of schizophrenia patients. Neurosci. Res. 77(4), 208-214 (2013).
47. Guizzetti M, Moore NH, Giordano G, Costa LG. Modulation of neuritogenesis by astrocyte muscarinic receptors. J. Biol. Chem. 283(46), 31884-31897 (2008).
48. VanDeMark KL, Guizzetti M, Giordano G, Costa LG. The activation of M1 muscarinic receptor signaling induces neuronal differentiation in pyramidal hippocampal neurons. J. Pharmacol. Exp. Ther. 329(2), 532-542 (2009).
49. Jiang X, Tian F, Mearow K, Okagaki P, Lipsky RH, Marini AM. The excitoprotective effect of N-methyl-d-aspartate receptors is mediated by a brain-derived neurotrophic factor autocrine loop in cultured hippocampal neurons. J. Neurochem. 94(3), 713-722 (2005).
50. Szulwach KE, Li X, Li Y et al. 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat. Neurosci. 14(12), 1607-1616 (2011).
51. Lister R, Mukamel EA, Nery JR et al. Global epigenomic reconfiguration during mammalian brain development. Science 341(6146), 1237905 (2013).
52. Jin SG, Wu X, Li AX, Pfeifer GP. Genomic mapping of 5-hydroxymethylcytosine in the human brain. Nucleic Acids Res. 39(12), 5015-5024 (2011).
53. Hahn MA, Qiu R, Wu X et al. Dynamics of 5-hydroxymethylcytosine and chromatin marks in Mammalian neurogenesis. Cell. Rep. 3(2), 291-300 (2013).
54. Song CX, Szulwach KE, Fu Y et al. Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat. Biotechnol. 29(1), 68-72 (2011).
55. Mellen M, Ayata P, Dewell S, Kriaucionis S, Heintz N. MeCP2 binds to 5hmC enriched within active genes and accessible chromatin in the nervous system. Cell 151(7), 1417-1430 (2012).
56. Wen L, Li X, Yan L et al. Whole-genome analysis of 5-hydroxymethylcytosine and 5-methylcytosine at base resolution in the human brain. Genome Biol. 15(3), R49 (2014).
57. Sun Z, Terragni J, Borgaro JG et al. High-resolution enzymatic mapping of genomic 5-hydroxymethylcytosine in mouse embryonic stem cells. Cell. Rep. 3(2), 567-576 (2013).
58. Yu M, Hon GC, Szulwach KE et al. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 149(6), 1368-1380 (2012).
59. Sharma RP, Tun N, Grayson DR. Depolarization induces downregulation of DNMT1 and DNMT3a in primary cortical cultures. Epigenetics 3(2), 74-80 (2008).
60. Anway MD, Leathers C, Skinner MK. Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology 147(12), 5515-5523 (2006).
61. Heijmans BT, Tobi EW, Stein AD et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl Acad. Sci. USA 105(44), 17046-17049 (2008).
62. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat. Genet. 23(3), 314-318 (1999).
63. Rakyan VK, Chong S, Champ ME et al. Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc. Natl Acad. Sci. USA 100(5), 2538-2543 (2003).