Generic placeholder image

Current Neurovascular Research

Author(s): Samira Silva Valvassori*, Roger Bitencourt Varela, Wilson Rodrigues Resende, Taise Possamai-Della, Laura de Araujo Borba, João Paulo Behenck, Gislaine Zilli Réus and João Quevedo

DOI: 10.2174/0115672026277345240115101852

DownloadDownload PDF Flyer Cite As
Antidepressant Effect of Sodium Butyrate is Accompanied by Brain Epigenetic Modulation in Rats Subjected to Early or Late Life Stress

Page: [586 - 598] Pages: 13

  • * (Excluding Mailing and Handling)

Abstract

Background: Major depression has a complex and multifactorial etiology constituted by the interaction between genetic and environmental factors in its development.

Objective: The aim of this study was to evaluate the effects of sodium butyrate (SD) on epigenetic enzyme alterations in rats subjected to animal models of depression induced by maternal deprivation (MD) or chronic mild stress (CMS).

Methods: To induce MD, male Wistar rats were deprived of maternal care during the first 10 days of life. To induce CMS, rats were subjected to the CMS for 40 days. Adult rats were then treated with daily injections of SD for 7 days. Animals were subjected to the forced swimming test (FST), and then, histone deacetylase (HDAC), histone acetyltransferase (HAT), and DNA methyltransferase (DNMT) activities were evaluated in the brain.

Results: MD and CMS increased immobility time in FST and increased HDAC and DNMT activity in the animal brains. SD reversed increased immobility induced by both animal models and the alterations in HDAC and DNMT activities. There was a positive correlation between enzyme activities and immobility time for both models. HDAC and DNMT activities also presented a positive correlation between themselves.

Conclusion: These results suggest that epigenetics can play an important role in major depression pathophysiology triggered by early or late life stress and its treatment.

[1]
Ferrari AJ, Somerville AJ, Baxter AJ, et al. Global variation in the prevalence and incidence of major depressive disorder: A systematic review of the epidemiological literature. Psychol Med 2013; 43(3): 471-81.
[http://dx.doi.org/10.1017/S0033291712001511] [PMID: 22831756]
[2]
Kessler RC, Bromet EJ. The epidemiology of depression across cultures. Annu Rev Public Health 2013; 34(1): 119-38.
[http://dx.doi.org/10.1146/annurev-publhealth-031912-114409] [PMID: 23514317]
[3]
Greenberg PE, Fournier AA, Sisitsky T, Pike CT, Kessler RC. The economic burden of adults with major depressive disorder in the United States (2005 and 2010). J Clin Psychiatry 2015; 76(2): 155-62.
[http://dx.doi.org/10.4088/JCP.14m09298] [PMID: 25742202]
[4]
American Psychiatric Association. Diagnostic and statistical manual of mental disorders. (5th ed.), American Psychiatric Publishing 2013.
[5]
Klengel T, Binder EB. Epigenetics of stress-related psychiatric disorders and gene × environment interactions. Neuron 2015; 86(6): 1343-57.
[http://dx.doi.org/10.1016/j.neuron.2015.05.036] [PMID: 26087162]
[6]
Nestler EJ, Peña CJ, Kundakovic M, Mitchell A, Akbarian S. Epigenetic basis of mental illness. Neuroscientist 2016; 22(5): 447-63.
[http://dx.doi.org/10.1177/1073858415608147] [PMID: 26450593]
[7]
Ludwig B, Dwivedi Y. Dissecting bipolar disorder complexity through epigenomic approach. Mol Psychiatry 2016; 21(11): 1490-8.
[http://dx.doi.org/10.1038/mp.2016.123] [PMID: 27480490]
[8]
Hoffmann A, Sportelli V, Ziller M, Spengler D. Epigenomics of major depressive disorders and schizophrenia: Early life decides. Int J Mol Sci 2017; 18(8): 1711.
[http://dx.doi.org/10.3390/ijms18081711] [PMID: 28777307]
[9]
Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotechnol 2010; 28(10): 1057-68.
[http://dx.doi.org/10.1038/nbt.1685] [PMID: 20944598]
[10]
Luczak MW. Jagodziński PP. The role of DNA methylation in cancer development. Folia Histochem Cytobiol 2006; 44(3): 143-54.
[PMID: 16977793]
[11]
Mitrousis N, Tropepe V, Hermanson O. Post-translational modifications of histones in vertebrate neurogenesis. Front Neurosci 2015; 9: 483.
[http://dx.doi.org/10.3389/fnins.2015.00483] [PMID: 26733796]
[12]
Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res 2011; 21(3): 381-95.
[http://dx.doi.org/10.1038/cr.2011.22] [PMID: 21321607]
[13]
Montejo AL, Montejo L, Navarro-Cremades F. Sexual side-effects of antidepressant and antipsychotic drugs. Curr Opin Psychiatry 2015; 28(6): 418-23.
[http://dx.doi.org/10.1097/YCO.0000000000000198] [PMID: 26382168]
[14]
David DJ, Gourion D. Antidepressant and tolerance: Determinants and management of major side effects. Encephale 2016; 42(6): 553-61.
[http://dx.doi.org/10.1016/j.encep.2016.05.006] [PMID: 27423475]
[15]
Mrazek DA, Hornberger JC, Altar CA, Degtiar I. A review of the clinical, economic, and societal burden of treatment-resistant depression: 1996-2013. Psychiatr Serv 2014; 65(8): 977-87.
[http://dx.doi.org/10.1176/appi.ps.201300059] [PMID: 24789696]
[16]
Shim I, Woo Y, Kim MD, Bahk WM. Antidepressants and mood stabilizers: Novel research avenues and clinical insights for bipolar depression. Int J Mol Sci 2017; 18(11): 2406.
[http://dx.doi.org/10.3390/ijms18112406] [PMID: 29137178]
[17]
Schroeder FA, Lin CL, Crusio WE, Akbarian S. Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse. Biol Psychiatry 2007; 62(1): 55-64.
[http://dx.doi.org/10.1016/j.biopsych.2006.06.036] [PMID: 16945350]
[18]
Zhu H, Huang Q, Xu H, Niu L, Zhou JN. Antidepressant-like effects of sodium butyrate in combination with estrogen in rat forced swimming test: Involvement of 5-HT1A receptors. Behav Brain Res 2009; 196(2): 200-6.
[http://dx.doi.org/10.1016/j.bbr.2008.08.039] [PMID: 18817816]
[19]
Valvassori S, Varela R, Arent C, et al. Sodium butyrate functions as an antidepressant and improves cognition with enhanced neurotrophic expression in models of maternal deprivation and chronic mild stress. Curr Neurovasc Res 2014; 11(4): 359-66.
[http://dx.doi.org/10.2174/1567202611666140829162158] [PMID: 25233278]
[20]
Kakoty V, Kc S, Yang CH, Dubey SK, Taliyan R. Exploring the epigenetic regulated modulation of fibroblast growth factor 21 involvement in high-fat diet associated Parkinson’s disease in rats. ACS Chem Neurosci 2023; 14(4): 725-40.
[http://dx.doi.org/10.1021/acschemneuro.2c00659] [PMID: 36694924]
[21]
Maejima H, Okamura M, Inoue T, Takamatsu Y, Nishio T, Liu Y. Epigenetic modifications in the motor cortex caused by exercise or pharmacological inhibition of histone deacetylases (HDACs) after intracerebral hemorrhage (ICH). Brain Res 2023; 1806: 148286.
[http://dx.doi.org/10.1016/j.brainres.2023.148286] [PMID: 36801267]
[22]
Varela RB, Resende WR, Dal-Pont GC, et al. Role of epigenetic regulatory enzymes in animal models of mania induced by amphetamine and paradoxical sleep deprivation. Eur J Neurosci 2021; 53(2): 649-62.
[http://dx.doi.org/10.1111/ejn.14922] [PMID: 32735698]
[23]
Valvassori SS, Budni J, Varela RB, Quevedo J. Contributions of animal models to the study of mood disorders. Rev Bras Psiquiatr 2013; 35 (Suppl. 2): S121-31.
[http://dx.doi.org/10.1590/1516-4446-2013-1168] [PMID: 24271224]
[24]
Levine S. Maternal and environmental influences on the adrenocortical response to stress in weanling rats. Science 1967; 156(3772): 258-60.
[http://dx.doi.org/10.1126/science.156.3772.258] [PMID: 6021047]
[25]
Katz RJ. Animal models and human depressive disorders. Neurosci Biobehav Rev 1981; 5(2): 231-46.
[http://dx.doi.org/10.1016/0149-7634(81)90004-X] [PMID: 7022272]
[26]
Réus GZ, Abelaira HM, dos Santos MAB, et al. Ketamine and imipramine in the nucleus accumbens regulate histone deacetylation induced by maternal deprivation and are critical for associated behaviors. Behav Brain Res 2013; 256: 451-6.
[http://dx.doi.org/10.1016/j.bbr.2013.08.041] [PMID: 24004850]
[27]
Mello PB, Benetti F, Cammarota M, Izquierdo I. Physical exercise can reverse the deficit in fear memory induced by maternal deprivation. Neurobiol Learn Mem 2009; 92(3): 364-9.
[http://dx.doi.org/10.1016/j.nlm.2009.04.004] [PMID: 19398029]
[28]
Resende WR, Valvassori SS, Réus GZ, et al. Effects of sodium butyrate in animal models of mania and depression. Behav Pharmacol 2013; 24(7): 569-79.
[http://dx.doi.org/10.1097/FBP.0b013e32836546fc] [PMID: 23994816]
[29]
Gamaro G, Manoli LP, Torres IL, Silveira R, Dalmaz C. Effects of chronic variate stress on feeding behavior and on monoamine levels in different rat brain structures. Neurochem Int 2003; 42(2): 107-14.
[http://dx.doi.org/10.1016/S0197-0186(02)00080-3] [PMID: 12421590]
[30]
Porsolt RD, Le Pichon M, Jalfre M. Depression: A new animal model sensitive to antidepressant treatments. Nature 1977; 266(5604): 730-2.
[http://dx.doi.org/10.1038/266730a0] [PMID: 559941]
[31]
Glowinski J, Iversen LL. Regional studies of catecholamines in the rat brain. I. The disposition of (3H)norepinephrine, (3H)dopamine and (3H)dopa in various regions of the brain. J Neurochem 1966; 13(8): 655-69.
[http://dx.doi.org/10.1111/j.1471-4159.1966.tb09873.x] [PMID: 5950056]
[32]
Chiu K, Lau WM, Lau HT, So KF, Chang RCC. Micro-dissection of rat brain for RNA or protein extraction from specific brain region. J Visual Experim 2007; 30(7)
[33]
Lowry O, Rosebrough N, Farr AL, Randall R. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193(1): 265-75.
[http://dx.doi.org/10.1016/S0021-9258(19)52451-6] [PMID: 14907713]
[34]
Vetulani J. Early maternal separation: A rodent model of depression and a prevailing human condition. Pharmacol Rep 2013; 65(6): 1451-61.
[http://dx.doi.org/10.1016/S1734-1140(13)71505-6] [PMID: 24552992]
[35]
Willner P. The chronic mild stress (CMS) model of depression: History, evaluation and usage. Neurobiol Stress 2017; 6: 78-93.
[http://dx.doi.org/10.1016/j.ynstr.2016.08.002] [PMID: 28229111]
[36]
Maciel AL, Abelaira HM, de Moura AB, et al. Acute treatment with ketamine and chronic treatment with minocycline exert antidepressant-like effects and antioxidant properties in rats subjected different stressful events. Brain Res Bull 2018; 137: 204-16.
[http://dx.doi.org/10.1016/j.brainresbull.2017.12.005] [PMID: 29253605]
[37]
Shepard RD, Langlois LD, Browne CA, Berenji A, Lucki I, Nugent FS. Ketamine reverses lateral habenula neuronal dysfunction and behavioral immobility in the forced swim test following maternal deprivation in late adolescent rats. Front Synaptic Neurosci 2018; 10: 39.
[http://dx.doi.org/10.3389/fnsyn.2018.00039] [PMID: 30425634]
[38]
Réus GZ, Maciel AL, Abelaira HM, et al. ω-3 and folic acid act against depressive-like behavior and oxidative damage in the brain of rats subjected to early- or late-life stress. Nutrition 2018; 53: 120-33.
[http://dx.doi.org/10.1016/j.nut.2018.03.006] [PMID: 29783176]
[39]
Shen J, Qu C, Xu L, Sun H, Zhang J. Resveratrol exerts a protective effect in chronic unpredictable mild stress–induced depressive-like behavior: Involvement of the AKT/GSK3β signaling pathway in hippocampus. Psychopharmacology 2019; 236(2): 591-602.
[http://dx.doi.org/10.1007/s00213-018-5087-1] [PMID: 30374891]
[40]
Molendijk ML, de Kloet ER. Forced swim stressor: Trends in usage and mechanistic consideration. Eur J Neurosci 2022; 55(9-10): 2813-31.
[http://dx.doi.org/10.1111/ejn.15139] [PMID: 33548153]
[41]
Stepanichev MY, Tishkina AO, Novikova MR, et al. Anhedonia but not passive floating is an indicator of depressive-like behavior in two chronic stress paradigms. Acta Neurobiol Exp 2016; 76(4): 324-33.
[http://dx.doi.org/10.21307/ane-2017-031] [PMID: 28094823]
[42]
Steckert AV, Dominguini D, Michels M, et al. The impact of chronic mild stress on long-term depressive behavior in rats which have survived sepsis. J Psychiatr Res 2017; 94: 47-53.
[http://dx.doi.org/10.1016/j.jpsychires.2017.06.006] [PMID: 28662375]
[43]
Guan J, Ding Y, Rong Y, et al. Early life stress increases brain glutamate and induces neurobehavioral manifestations in rats. ACS Chem Neurosci 2020; 11(24): 4169-78.
[http://dx.doi.org/10.1021/acschemneuro.0c00454] [PMID: 33179901]
[44]
Cryan JF, Markou A, Lucki I. Assessing antidepressant activity in rodents: Recent developments and future needs. Trends Pharmacol Sci 2002; 23(5): 238-45.
[http://dx.doi.org/10.1016/S0165-6147(02)02017-5] [PMID: 12008002]
[45]
Cryan JF, Valentino RJ, Lucki I. Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci Biobehav Rev 2005; 29(4-5): 547-69.
[http://dx.doi.org/10.1016/j.neubiorev.2005.03.008] [PMID: 15893822]
[46]
Kokras N, Antoniou K, Mikail HG, Kafetzopoulos V, Papadopoulou-Daifoti Z, Dalla C. Forced swim test: What about females? Neuropharmacology 2015; 99: 408-21.
[http://dx.doi.org/10.1016/j.neuropharm.2015.03.016] [PMID: 25839894]
[47]
Jawahar MC, Murgatroyd C, Harrison EL, Baune BT. Epigenetic alterations following early postnatal stress: A review on novel aetiological mechanisms of common psychiatric disorders. Clin Epigenetics 2015; 7(1): 122.
[http://dx.doi.org/10.1186/s13148-015-0156-3] [PMID: 26583053]
[48]
Park SW, Lee JG, Seo MK, et al. Epigenetic modification of glucocorticoid receptor promoter I7 in maternally separated and restraint-stressed rats. Neurosci Lett 2017; 650: 38-44.
[http://dx.doi.org/10.1016/j.neulet.2017.04.024] [PMID: 28414132]
[49]
Seo MK, Kim S, Seog DH, et al. Effects of early life stress on epigenetic changes of the glucocorticoid receptor 17 promoter during adulthood. Int J Mol Sci 2020; 21(17): 6331.
[http://dx.doi.org/10.3390/ijms21176331] [PMID: 32878311]
[50]
Shepard RD, Langlois LD, Authement ME, Nugent FS. Histone deacetylase inhibition reduces ventral tegmental area dopamine neuronal hyperexcitability involving AKAP150 signaling following maternal deprivation in juvenile male rats. J Neurosci Res 2020; 98(7): 1457-67.
[http://dx.doi.org/10.1002/jnr.24613] [PMID: 32162391]
[51]
Levine A, Worrell TR, Zimnisky R, Schmauss C. Early life stress triggers sustained changes in histone deacetylase expression and histone H4 modifications that alter responsiveness to adolescent antidepressant treatment. Neurobiol Dis 2012; 45(1): 488-98.
[http://dx.doi.org/10.1016/j.nbd.2011.09.005] [PMID: 21964251]
[52]
Suri D, Bhattacharya A, Vaidya VA. Early stress evokes temporally distinct consequences on the hippocampal transcriptome, anxiety and cognitive behaviour. Int J Neuropsychopharmacol 2014; 17(2): 289-301.
[http://dx.doi.org/10.1017/S1461145713001004] [PMID: 24025219]
[53]
Albuquerque Filho MO, de Freitas BS, Garcia RCL, Crivelaro PCF, Schröder N, de Lima MNM. Dual influences of early-life maternal deprivation on histone deacetylase activity and recognition memory in rats. Neuroscience 2017; 344: 360-70.
[http://dx.doi.org/10.1016/j.neuroscience.2016.12.054] [PMID: 28089578]
[54]
Pusalkar M, Suri D, Kelkar A, Bhattacharya A, Galande S, Vaidya VA. Early stress evokes dysregulation of histone modifiers in the medial prefrontal cortex across the life span. Dev Psychobiol 2016; 58(2): 198-210.
[http://dx.doi.org/10.1002/dev.21365] [PMID: 26395029]
[55]
Ferland CL, Schrader LA. Regulation of histone acetylation in the hippocampus of chronically stressed rats: A potential role of sirtuins. Neuroscience 2011; 174: 104-14.
[http://dx.doi.org/10.1016/j.neuroscience.2010.10.077] [PMID: 21056634]
[56]
Benoit JD, Rakic P, Frick KM. Prenatal stress induces spatial memory deficits and epigenetic changes in the hippocampus indicative of heterochromatin formation and reduced gene expression. Behav Brain Res 2015; 281: 1-8.
[http://dx.doi.org/10.1016/j.bbr.2014.12.001] [PMID: 25496779]
[57]
Al Shoyaib A, Archie SR, Karamyan VT. Intraperitoneal route of drug administration: Should it be used in experimental animal studies? Pharm Res 2020; 37(1): 12.
[http://dx.doi.org/10.1007/s11095-019-2745-x] [PMID: 31873819]
[58]
Moloney RD, Stilling RM, Dinan TG, Cryan JF. Early-life stress-induced visceral hypersensitivity and anxiety behavior is reversed by histone deacetylase inhibition. Neurogastroenterol Motil 2015; 27(12): 1831-6.
[http://dx.doi.org/10.1111/nmo.12675] [PMID: 26403543]
[59]
Shepard RD, Gouty S, Kassis H, et al. Targeting histone deacetylation for recovery of maternal deprivation-induced changes in BDNF and AKAP150 expression in the VTA. Exp Neurol 2018; 309: 160-8.
[http://dx.doi.org/10.1016/j.expneurol.2018.08.002] [PMID: 30102916]
[60]
Peleg S, Feller C, Ladurner AG, Imhof A. The metabolic impact on histone acetylation and transcription in ageing. Trends Biochem Sci 2016; 41(8): 700-11.
[http://dx.doi.org/10.1016/j.tibs.2016.05.008] [PMID: 27283514]
[61]
Morris MJ, Na ES, Autry AE, Monteggia LM. Impact of DNMT1 and DNMT3a forebrain knockout on depressive- and anxiety like behavior in mice. Neurobiol Learn Mem 2016; 135: 139-45.
[http://dx.doi.org/10.1016/j.nlm.2016.08.012] [PMID: 27545441]
[62]
Ignácio ZM, Réus GZ, Abelaira HM, et al. Quetiapine treatment reverses depressive-like behavior and reduces DNA methyltransferase activity induced by maternal deprivation. Behav Brain Res 2017; 320: 225-32.
[http://dx.doi.org/10.1016/j.bbr.2016.11.044] [PMID: 27913254]
[63]
Boku S, Toda H, Nakagawa S, et al. Neonatal maternal separation alters the capacity of adult neural precursor cells to differentiate into neurons via methylation of retinoic acid receptor gene promoter. Biol Psychiatry 2015; 77(4): 335-44.
[http://dx.doi.org/10.1016/j.biopsych.2014.07.008] [PMID: 25127741]
[64]
Park SW, Seo MK, Lee JG, Hien LT, Kim YH. Effects of maternal separation and antidepressant drug on epigenetic regulation of the brain-derived neurotrophic factor exon I promoter in the adult rat hippocampus. Psychiatry Clin Neurosci 2018; 72(4): 255-65.
[http://dx.doi.org/10.1111/pcn.12609] [PMID: 28990703]
[65]
Weaver ICG, Cervoni N, Champagne FA, et al. Epigenetic programming by maternal behavior. Nat Neurosci 2004; 7(8): 847-54.
[http://dx.doi.org/10.1038/nn1276] [PMID: 15220929]
[66]
Hu J, Cao S, Zhang Z, et al. Effects of caffeic acid on epigenetics in the brain of rats with chronic unpredictable mild stress. Mol Med Rep 2020; 22(6): 5358-68.
[http://dx.doi.org/10.3892/mmr.2020.11609] [PMID: 33173990]
[67]
Xiang D, Sun S, Wang G, Liu Z. Effects of CRMP2 DNA methylation in the hippocampus on depressive-like behaviors and cytoskeletal proteins in rats. Front Cell Neurosci 2021; 15: 644663.
[http://dx.doi.org/10.3389/fncel.2021.644663] [PMID: 33815064]
[68]
Sales AJ, Joca SRL. Antidepressant administration modulates stress-induced DNA methylation and DNA methyltransferase expression in rat prefrontal cortex and hippocampus. Behav Brain Res 2018; 343: 8-15.
[http://dx.doi.org/10.1016/j.bbr.2018.01.022] [PMID: 29378290]
[69]
Xiang D, Xiao J, Sun S, et al. Differential regulation of DNA methylation at the CRMP2 promoter region between the hippocampus and prefrontal cortex in a CUMS depression model. Front Psychiatry 2020; 11: 141.
[http://dx.doi.org/10.3389/fpsyt.2020.00141] [PMID: 32256396]
[70]
Niknazar S, Nahavandi A, Peyvandi AA, Peyvandi H, Akhtari AS, Karimi M. Comparison of the adulthood chronic stress effect on hippocampal BDNF signaling in male and female rats. Mol Neurobiol 2016; 53(6): 4026-33.
[http://dx.doi.org/10.1007/s12035-015-9345-5] [PMID: 26189832]
[71]
Wigner P, Synowiec E, Czarny P, et al. Effects of venlafaxine on the expression level and methylation status of genes involved in oxidative stress in rats exposed to a chronic mild stress. J Cell Mol Med 2020; 24(10): 5675-94.
[http://dx.doi.org/10.1111/jcmm.15231] [PMID: 32281745]
[72]
Wigner P, Synowiec E. Jóźwiak P, et al. The changes of expression and methylation of genes involved in oxidative stress in course of chronic mild stress and antidepressant therapy with agomelatine. Genes 2020; 11(6): 644.
[http://dx.doi.org/10.3390/genes11060644] [PMID: 32545212]
[73]
Erburu M, Cajaleon L, Guruceaga E, et al. Chronic mild stress and imipramine treatment elicit opposite changes in behavior and in gene expression in the mouse prefrontal cortex. Pharmacol Biochem Behav 2015; 135: 227-36.
[http://dx.doi.org/10.1016/j.pbb.2015.06.001] [PMID: 26051025]
[74]
Kv A, Madhana RM, Js IC, Lahkar M, Sinha S, Naidu VGM. Antidepressant activity of vorinostat is associated with amelioration of oxidative stress and inflammation in a corticosterone-induced chronic stress model in mice. Behav Brain Res 2018; 344: 73-84.
[http://dx.doi.org/10.1016/j.bbr.2018.02.009] [PMID: 29452193]
[75]
Golden SA, Christoffel DJ, Heshmati M, et al. Epigenetic regulation of RAC1 induces synaptic remodeling in stress disorders and depression. Nat Med 2013; 19(3): 337-44.
[http://dx.doi.org/10.1038/nm.3090] [PMID: 23416703]
[76]
Authement ME, Kodangattil JN, Gouty S, et al. Histone deacetylase inhibition rescues maternal deprivation-induced gabaergic metaplasticity through restoration of akap Signaling. Neuron 2015; 86(5): 1240-52.
[http://dx.doi.org/10.1016/j.neuron.2015.05.024] [PMID: 26050042]
[77]
Le François B, Soo J, Millar AM, et al. Chronic mild stress and antidepressant treatment alter 5-HT1A receptor expression by modifying DNA methylation of a conserved Sp4 site. Neurobiol Dis 2015; 82: 332-41.
[http://dx.doi.org/10.1016/j.nbd.2015.07.002] [PMID: 26188176]
[78]
Elliott E, Ezra-Nevo G, Regev L, Neufeld-Cohen A, Chen A. Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice. Nat Neurosci 2010; 13(11): 1351-3.
[http://dx.doi.org/10.1038/nn.2642] [PMID: 20890295]
[79]
Wang CH, Zhang XL, Li Y, et al. Role of hippocampus mitogen-activated protein kinase phosphatase-1 mRNA expression and DNA methylation in the depression of the rats with chronic unpredicted stress. Cell Mol Neurobiol 2015; 35(4): 473-82.
[http://dx.doi.org/10.1007/s10571-014-0141-y] [PMID: 25410305]
[80]
Ju LS, Yang JJ, Lei L, et al. The combination of long-term ketamine and extinction training contributes to fear erasure by bdnf methylation. Front Cell Neurosci 2017; 11: 100.
[http://dx.doi.org/10.3389/fncel.2017.00100] [PMID: 28473755]
[81]
Jones PL, Veenstra GJC, Wade PA, et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 1998; 19(2): 187-91.
[http://dx.doi.org/10.1038/561] [PMID: 9620779]
[82]
Nan X, Ng HH, Johnson CA, et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998; 393(6683): 386-9.
[http://dx.doi.org/10.1038/30764] [PMID: 9620804]
[83]
Dobosy JR, Selker EU. Emerging connections between DNA methylation and histone acetylation. Cell Mol Life Sci 2001; 58(5): 721-7.
[http://dx.doi.org/10.1007/PL00000895] [PMID: 11437233]
[84]
Fuks F, Burgers WA, Brehm A, Hughes-Davies L, Kouzarides T. DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat Genet 2000; 24(1): 88-91.
[http://dx.doi.org/10.1038/71750] [PMID: 10615135]
[85]
Fuks F, Hurd PJ, Wolf D, Nan X, Bird AP, Kouzarides T. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem 2003; 278(6): 4035-40.
[http://dx.doi.org/10.1074/jbc.M210256200] [PMID: 12427740]
[86]
Robertson KD, Ait-Si-Ali S, Yokochi T, Wade PA, Jones PL, Wolffe AP. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat Genet 2000; 25(3): 338-42.
[http://dx.doi.org/10.1038/77124] [PMID: 10888886]
[87]
Rountree MR, Bachman KE, Baylin SB. DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat Genet 2000; 25(3): 269-77.
[http://dx.doi.org/10.1038/77023] [PMID: 10888872]