Repeated treatment with electroconvulsive seizures induces HDAC2 expression and down-regulation of NMDA receptor-related genes through histone deacetylation in the rat frontal cortex

International Journal of Neuropsychopharmacology

Volumn 17, Issue 9, 2014, Pages 1487-1500

  Park, Hong Geun ^a,b   Yu, Hyun Sook ^a,b   Park, Soyoung ^a   Ahn, Yong Min ^a,b,c   Kim, Yong Sik ^d   Kim, Se Hyun ^a,c  

^a Seoul National University Hospital   (South Korea)

^b Seoul National University College of Medicine   (South Korea)

^c Seoul National University   (South Korea)

^d Dongguk University Ilsan Hospital   (South Korea)

Author keywords

ECS; HDAC; histone acetylation; synaptic plasticity genes

Indexed keywords

BUTYRIC ACID; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE H3; HISTONE H4; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NABU; UNCLASSIFIED DRUG; ANTIHISTAMINIC AGENT; ENOLASE; GLIAL FIBRILLARY ACIDIC PROTEIN; HDAC2 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II ALPHA GENE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; EARLY GROWTH RESPONSE FACTOR 1 GENE; ELECTROCONVULSIVE SEIZURE; FRONTAL CORTEX; GENE; GENE EXPRESSION; GENE TARGETING; HISTONE ACETYLATION; MALE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A GENE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B GENE; NEURITIN1 GENE; NONHUMAN; ONCOGENE C FOS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT; SEIZURE; UPREGULATION; ACETYLATION; ANALYSIS OF VARIANCE; ANIMAL; DISEASE MODEL; DRUG EFFECTS; ELECTROSHOCK; ENZYMOLOGY; FRONTAL LOBE; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY; SEIZURES; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ACETYLATION; ANALYSIS OF VARIANCE; ANIMALS; BUTYRIC ACID; CHROMATIN IMMUNOPRECIPITATION; DISEASE MODELS, ANIMAL; ELECTROSHOCK; FRONTAL LOBE; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; HISTAMINE ANTAGONISTS; HISTONE DEACETYLASE 2; MALE; PHOSPHOPYRUVATE HYDRATASE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, MESSENGER; SEIZURES; SIGNAL TRANSDUCTION;

EID: 84904893871     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145714000248     Document Type: Article

References (86)

1. Abel T, Zukin RS (2008) Epigenetic targets of HDAC inhibition in neurodegenerative and psychiatric disorders. Curr Opin Pharmacol 8:57-64.
2. Akbarian S, Ruehl MG, Bliven E, Luiz LA, Peranelli AC, Baker SP, Roberts RC, Bunney WE Jr., Conley RC, Jones EG, Tamminga CA, Guo Y (2005) Chromatin alterations associated with down-regulated metabolic gene expression in the prefrontal cortex of subjects with schizophrenia. Arch Gen Psychiatry 62:829-840.
3. Akhtar MW, Raingo J, Nelson ED, Montgomery RL, Olson EN, Kavalali ET, Monteggia LM (2009) Histone deacetylases 1 and 2 form a developmental switch that controls excitatory synapse maturation and function. J Neurosci 29:8288-8297.
4. Altar CA, Laeng P, Jurata LW, Brockman JA, Lemire A, Bullard J, Bukhman YV, Young TA, Charles V, Palfreyman MG (2004) Electroconvulsive seizures regulate gene expression of distinct neurotrophic signaling pathways. J Neurosci 24:2667-2677.
5. Bayer KU, De Koninck P, Leonard AS, Hell JW, Schulman H (2001) Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature 411:801-805.
6. Beckmann AM, Wilce PA (1997) Egr transcription factors in the nervous system. Neurochem Int 31:477-510; Discussion 517-476.
7. Boks MP, de Jong NM, Kas MJ, Vinkers CH, Fernandes C, Kahn RS, Mill J, Ophoff RA (2012) Current status and future prospects for epigenetic psychopharmacology. Epigenetics 7:20-28.
8. Broide RS, Redwine JM, Aftahi N, Young W, Bloom FE, Winrow CJ (2007) Distribution of histone deacetylases 1-11 in the rat brain. J Mol Neurosci 31:47-58.
9. Caplan G (1946) Electrical convulsion therapy in the treatment of epilepsy. J Ment Sci 92:784-793.
10. Carew JS, Giles FJ, Nawrocki ST (2008) Histone deacetylase inhibitors: mechanisms of cell death and promise in combination cancer therapy. Cancer Lett 269:7-17.
11. Cassel S, Carouge D, Gensburger C, Anglard P, Burgun C, Dietrich JB, Aunis D, Zwiller J (2006) Fluoxetine and cocaine induce the epigenetic factors MeCP2 and MBD1 in adult rat brain. Mol Pharmacol 70:487-492.
12. Chakrabarti SK, James JC, Mirmira RG (2002) Quantitative assessment of gene targeting in vitro and in vivo by the pancreatic transcription factor, Pdx1. Importance of chromatin structure in directing promoter binding. J Biol Chem 277:13286-13293.
13. Coskun V, Tsoa R, Sun YE (2012) Epigenetic regulation of stem cells differentiating along the neural lineage. Curr Opin Neurobiol 22:762-767.
14. Covington HE III, Maze I, LaPlant QC, Vialou VF, Ohnishi YN, Berton O, Fass DM, Renthal W, Rush AJ III, Wu EY, Ghose S, Krishnan V, Russo SJ, Tamminga C, Haggarty SJ, Nestler EJ (2009) Antidepressant actions of histone deacetylase inhibitors. J Neurosci 29:11451-11460.
15. Crowe SL, Tsukerman S, Gale K, Jorgensen TJ, Kondratyev AD (2011) Phosphorylation of histone H2A.X as an early marker of neuronal endangerment following seizures in the adult rat brain. J Neurosci 31:7648-7656.
16. de Ruijter AJ, van Gennip AH, Caron HN, Kemp S, van Kuilenburg AB (2003) Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 370:737-749.
17. Dyrvig M, Hansen HH, Christiansen SH, Woldbye DP, Mikkelsen JD, Lichota J (2012) Epigenetic regulation of Arc and c-Fos in the hippocampus after acute electroconvulsive stimulation in the rat. Brain Res Bull 88:507-513.
18. Fischer A, Sananbenesi F, Wang X, Dobbin M, Tsai LH (2007) Recovery of learning and memory is associated with chromatin remodelling. Nature 447:178-182.
19. Freeman WM, Patel KM, Brucklacher RM, Lull ME, Erwin M, Morgan D, Roberts DC, Vrana KE (2008) Persistent alterations in mesolimbic gene expression with abstinence from cocaine self-administration. Neuropsychopharmacology 33:1807-1817.
20. Fryland T, Elfving B, Christensen JH, Mors O, Wegener G, Borglum AD (2012) Electroconvulsive seizures regulates the Brd1 gene in the frontal cortex and hippocampus of the adult rat. Neurosci Lett 516:110-113.
21. Fujino T, Lee WC, Nedivi E (2003) Regulation of cpg15 by signaling pathways that mediate synaptic plasticity. Mol Cell Neurosci 24:538-554.
22. Fujino T, Wu Z, Lin WC, Phillips MA, Nedivi E (2008) cpg15 and cpg15-2 constitute a family of activity-regulated ligands expressed differentially in the nervous system to promote neurite growth and neuronal survival. J Comp Neurol 507:1831-1845.
23. Gavin DP, Kartan S, Chase K, Jayaraman S, Sharma RP (2009) Histone deacetylase inhibitors and candidate gene expression: an in vivo and in vitro approach to studying chromatin remodeling in a clinical population. J Psychiatr Res 43:870-876.
24. Goebel DJ, Poosch MS (1999) NMDA receptor subunit gene expression in the rat brain: a quantitative analysis of endogenous mRNA levels of NR1Com, NR2A, NR2B, NR2C, NR2D and NR3A. Brain Res Mol Brain Res 69:164-170.
25. Gottlicher M, Minucci S, Zhu P, Kramer OH, Schimpf A, Giavara S, Sleeman JP, Lo Coco F, Nervi C, Pelicci PG, Heinzel T (2001) Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J 20:6969-6978.
26. Graff J, Tsai LH (2013) Histone acetylation: molecular mnemonics on the chromatin. Nat Rev Neurosci 14:97-111.
27. Grozinger CM, Schreiber SL (2002) Deacetylase enzymes: biological functions and the use of small-molecule inhibitors. Chem Biol 9:3-16.
28. Guan JS, Haggarty SJ, Giacometti E, Dannenberg JH, Joseph N, Gao J, Nieland TJ, Zhou Y, Wang X, Mazitschek R, Bradner JE, DePinho RA, Jaenisch R, Tsai LH (2009) HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459:55-60.
29. Guidotti A, Dong E, Kundakovic M, Satta R, Grayson DR, Costa E (2009) Characterization of the action of antipsychotic subtypes on valproate-induced chromatin remodeling. Trends Pharmacol Sci 30:55-60.
30. Guzowski JF, Setlow B, Wagner EK, McGaugh JL (2001) Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J Neurosci 21:5089-5098.
31. Haggarty SJ, Tsai LH (2011) Probing the role of HDACs and mechanisms of chromatin-mediated neuroplasticity. Neurobiol Learn Mem 96:41-52.
32. Huang HL, Lee HY, Tsai AC, Peng CY, Lai MJ, Wang JC, Pan SL, Teng CM, Liou JP (2012a) Anticancer activity of MPT0E028, a novel potent histone deacetylase inhibitor, in human colorectal cancer HCT116 cells in vitro and in vivo. PLoS ONE 7:e43645. Doi:10.1371/journal.pone.0043645.
33. Huang Y, Zhao F, Wang L, Yin H, Zhou C, Wang X (2012b) Increased expression of histone deacetylases 2 in temporal lobe epilepsy: a study of epileptic patients and rat models. Synapse 66:151-159.
34. Hudmon A, Schulman H (2002) Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II. Biochem J 364:593-611.
35. Jiang Y, Langley B, Lubin FD, Renthal W, Wood MA, Yasui DH, Kumar A, Nestler EJ, Akbarian S, Beckel-Mitchener AC (2008) Epigenetics in the nervous system. J Neurosci 28:11753-11759.
36. Karamoysoyli E, Burnand RC, Tomlinson DR, Gardiner NJ (2008) Neuritin mediates nerve growth factor-induced axonal regeneration and is deficient in experimental diabetic neuropathy. Diabetes 57:181-189.
37. Kato N (2009) Neurophysiological mechanisms of electroconvulsive therapy for depression. Neurosci Res 64:3-11.
38. Kim BW, Yang S, Lee CH, Son H (2011) A critical time window for the survival of neural progenitor cells by HDAC inhibitors in the hippocampus. Mol Cells 31:159-164.
39. Kim SH, Yu HS, Park HG, Jeon WJ, Song JY, Kang UG, Ahn YM, Lee YH, Kim YS (2008) Dose-dependent effect of intracerebroventricular injection of ouabain on the phosphorylation of the MEK1/2-ERK1/2-p90RSK pathway in the rat brain related to locomotor activity. Prog Neuropsychopharmacol Biol Psychiatry 32:1637-1642.
40. Kim SH, Kim MK, Yu HS, Kim HS, Park IS, Park HG, Kang UG, Kim YS (2010) Electroconvulsive seizure increases phosphorylation of PKC substrates, including GAP-43, MARCKS, and neurogranin, in rat brain. Prog Neuropsychopharmacol Biol Psychiatry 34:115-121.
41. Kim SH, Yu HS, Park HG, Ha K, Kim YS, Shin SY, Ahn YM (2013) Intracerebroventricular administration of ouabain, a Na/ K-ATPase inhibitor, activates mTOR signal pathways and protein translation in the rat frontal cortex. Prog Neuropsychopharmacol Biol Psychiatry 45C:73-82.
42. Kramer OH (2009) HDAC2: a critical factor in health and disease. Trends Pharmacol Sci 30:647-655.
43. Kubista M, Akerman B, Norden B (1987) Characterization of interaction between DNA and 4?,6-diamidino-2-phenylindole by optical spectroscopy. Biochemistry 26:4545-4553.
44. Kurita M et al. (2012) HDAC2 regulates atypical antipsychotic responses through the modulation of mGlu2 promoter activity. Nat Neurosci 15:1245-1254.
45. Lahm A, Paolini C, Pallaoro M, Nardi MC, Jones P, Neddermann P, Sambucini S, Bottomley MJ, Lo Surdo P, Carfi A, Koch U, De Francesco R, Steinkuhler C, Gallinari P (2007) Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases. Proc Natl Acad Sci USA 104:17335-17340.
46. Levenson JM, Sweatt JD (2005) Epigenetic mechanisms in memory formation. Nat Rev Neurosci 6:108-118.
47. Levenson JM, O'Riordan KJ, Brown KD, Trinh MA, Molfese DL, Sweatt JD (2004) Regulation of histone acetylation during memory formation in the hippocampus. J Biol Chem 279:40545-40559.
48. Li J, Guo Y, Schroeder FA, Youngs RM, Schmidt TW, Ferris C, Konradi C, Akbarian S (2004) Dopamine D2-like antagonists induce chromatin remodeling in striatal neurons through cyclic AMP-protein kinase A and NMDA receptor signaling. J Neurochem 90:1117-1131.
49. Lisanby SH (2007) Electroconvulsive therapy for depression. N Engl J Med 357:1939-1945.
50. Lisman J, Schulman H, Cline H (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3:175-190.
51. Marwick JA, Kirkham PA, Stevenson CS, Danahay H, Giddings J, Butler K, Donaldson K, Macnee W, Rahman I (2004) Cigarette smoke alters chromatin remodeling and induces proinflammatory genes in rat lungs. Am J Respir Cell Mol Biol 31:633-642.
52. Merkl A, Heuser I, Bajbouj M (2009) Antidepressant electroconvulsive therapy: mechanism of action, recent advances and limitations. Exp Neurol 219:20-26.
53. Mikkelsen JD, Woldbye D, Kragh J, Larsen PJ, Bolwig TG (1994) Electroconvulsive shocks increase the expression of neuropeptide Y (NPY) mRNA in the piriform cortex and the dentate gyrus. Brain Res Mol Brain Res 23:317-322.
54. Mokin M, Keifer J (2005) Expression of the immediate-early gene-encoded protein Egr-1 (zif268) during in vitro classical conditioning. Learn Mem 12:144-149.
55. Montgomery RL, Hsieh J, Barbosa AC, Richardson JA, Olson EN (2009) Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development. Proc Natl Acad Sci USA 106:7876-7881.
56. Mukherjee S, Sackeim HA, Schnur DB (1994) Electroconvulsive therapy of acute manic episodes: a review of 50 years' experience. Am J Psychiatry 151:169-176.
57. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
58. Naeve GS, Ramakrishnan M, Kramer R, Hevroni D, Citri Y, Theill LE (1997) Neuritin: a gene induced by neural activity and neurotrophins that promotes neuritogenesis. Proc Natl Acad Sci USA 94:2648-2653.
59. Nedivi E, Wu GY, Cline HT (1998) Promotion of dendritic growth by CPG15, an activity-induced signaling molecule. Science 281:1863-1866.
60. Newton SS, Collier EF, Hunsberger J, Adams D, Terwilliger R, Selvanayagam E, Duman RS (2003) Gene profile of electroconvulsive seizures: induction of neurotrophic and angiogenic factors. J Neurosci 23:10841-10851.
61. Nott A, Watson PM, Robinson JD, Crepaldi L, Riccio A (2008) S-Nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature 455:411-415.
62. Ookubo M, Kanai H, Aoki H, Yamada N (2013) Antidepressants and mood stabilizers effects on histone deacetylase expression in C57BL/6 mice: brain region specific changes. J Psychiatr Res 47:1204-1214.
63. Park HG, Kim SH, Kim HS, Ahn YM, Kang UG, Kim YS (2011) Repeated electroconvulsive seizure treatment in rats reduces inducibility of early growth response genes and hyperactivity in response to cocaine administration. Prog Neuropsychopharmacol Biol Psychiatry 35:1014-1021.
64. Paxinos G, Watson C (1998) The rat brain in stereotactic coordinates, 4th edn. Sydney: Academic Press
65. Phiel CJ, Zhang F, Huang EY, Guenther MG, Lazar MA, Klein PS (2001) Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 276:36734-36741.
66. Ploski JE, Newton SS, Duman RS (2006) Electroconvulsive seizure-induced gene expression profile of the hippocampus dentate gyrus granule cell layer. J Neurochem 99:1122-1132.
67. Post RM, Putnam F, Contel NR, Goldman B (1984) Electroconvulsive seizures inhibit amygdala kindling: implications for mechanisms of action in affective illness. Epilepsia 25:234-239.
68. Raff MC, Fields KL, Hakomori SI, Mirsky R, Pruss RM, Winter J (1979) Cell-type-specific markers for distinguishing and studying neurons and the major classes of glial cells in culture. Brain Res 174:283-308.
69. Renthal W, Maze I, Krishnan V, Covington HE III, Xiao G, Kumar A, Russo SJ, Graham A, Tsankova N, Kippin TE, Kerstetter KA, Neve RL, Haggarty SJ, McKinsey TA, Bassel-Duby R, Olson EN, Nestler EJ (2007) Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56:517-529.
70. Sackeim HA (1999) The anticonvulsant hypothesis of the mechanisms of action of ECT: current status. J ECT 15:5-26.
71. Sackeim HA, Decina P, Prohovnik I, Malitz S, Resor SR (1983) Anticonvulsant and antidepressant properties of electroconvulsive therapy: a proposed mechanism of action. Biol Psychiatry 18:1301-1310.
72. Sanhueza M, Fernandez-Villalobos G, Stein IS, Kasumova G, Zhang P, Bayer KU, Otmakhov N, Hell JW, Lisman J (2011) Role of the CaMKII/NMDA receptor complex in the maintenance of synaptic strength. J Neurosci 31:9170-9178.
73. Schroeder FA, Lin CL, Crusio WE, Akbarian S (2007) Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse. Biol Psychiatry 62:55-64.
74. Segi-Nishida E (2011) Exploration of new molecular mechanisms for antidepressant actions of electroconvulsive seizure. Biol Pharm Bull 34:939-944.
75. Sharma RP, Rosen C, Kartan S, Guidotti A, Costa E, Grayson DR, Chase K (2006) Valproic acid and chromatin remodeling in schizophrenia and bipolar disorder: preliminary results from a clinical population. Schizophr Res 88:227-231.
76. Sharma RP, Grayson DR, Gavin DP (2008) Histone deactylase 1 expression is increased in the prefrontal cortex of schizophrenia subjects: analysis of the National Brain Databank microarray collection. Schizophr Res 98:111-117.
77. Stafford JM, Raybuck JD, Ryabinin AE, Lattal KM (2012) Increasing histone acetylation in the hippocampus-infralimbic network enhances fear extinction. Biol Psychiatry 72:25-33.
78. Sun J, Ming GL, Song H (2011) Epigenetic regulation of neurogenesis in the adult mammalian brain. Eur J Neurosci 33:1087-1093.
79. Tang B, Dean B, Thomas EA (2011) Disease- and age-related changes in histone acetylation at gene promoters in psychiatric disorders. Transl Psychiatry 1:e64. Doi: 10.1038/tp.2011.61.
80. Tharyan P, Adams CE (2005) Electroconvulsive therapy for schizophrenia. Cochrane Database Syst Rev CD000076
81. Tsankova NM, Kumar A, Nestler EJ (2004) Histone modifications at gene promoter regions in rat hippocampus after acute and chronic electroconvulsive seizures. J Neurosci 24:5603-5610.
82. Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ (2006) Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 9:519-525.
83. Tsankova NM, Renthal W, Kumar A, Nestler EJ (2007) Epigenetic regulation in psychiatric disorders. Nat Rev Neurosci 8:355-367.
84. Yang XJ, Seto E (2008) The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol 9:206-218.
85. Zhu P, Martin E, Mengwasser J, Schlag P, Janssen KP, Gottlicher M (2004) Induction of HDAC2 expression upon loss of APC in colorectal tumorigenesis. Cancer Cell 5:455-463.
86. Zimmermann S, Kiefer F, Prudenziati M, Spiller C, Hansen J, Floss T, Wurst W, Minucci S, Gottlicher M (2007) Reduced body size and decreased intestinal tumor rates in HDAC2-mutant mice. Cancer Res 67:9047-9054.