Epigenetic signaling in psychiatric disorders: Stress and depression

Dialogues in Clinical Neuroscience

Volumn 16, Issue 3, 2014, Pages 281-295

  Bagot, Rosemary C ^a   Labonté, Benoit ^a   Peña, Catherine J ^a   Nestler, Eric J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Acetylation; Animal model; Depression; Early life; Epigenetic; Histone; Methylation; Stress

Indexed keywords

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DEPRESSION; DNA METHYLATION; ENVIRONMENTAL FACTOR; EPIGENETICS; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; MENTAL DISEASE; NONHUMAN; REGULATORY MECHANISM; STRESS; GENE EXPRESSION; GENETIC EPIGENESIS; GENETICS; MENTAL STRESS; SIGNAL TRANSDUCTION;

DEPRESSION; EPIGENESIS, GENETIC; GENE EXPRESSION; HUMANS; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL;

EID: 84911394488     PISSN: 12948322     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (105)

1. Feng J, Nestler EJ. Epigenetic mechanisms of drug addiction. Curr Opin Neurobiol. 2013;23:521-528.
2. Pena CJ, Bagot RC, Labonte B, Nestler EJ. Epigenetic signaling in psychiatric disorders. J Mol Biol. 2014 Apr 5. Epub ahead of print.
3. Bali P, Kenny PJ. MicroRNAs and drug addiction. Front Genet. 2013;4:43.
4. Robison AJ, Nestler EJ. Transcriptional and epigenetic mechanisms of addiction. Nat Rev Neurosci. 2011;12:623-637.
5. Mahgoub M, Monteggia LM. Epigenetics and psychiatry. Neurotherapeutics. 2013;10:734-741.
6. Hasan A, Mitchell A, Schneider A, Halene T, Akbarian S. Epigenetic dysregulation in schizophrenia: molecular and clinical aspects of histone deacetylase inhibitors. Eur Arch Psychiatry Clin Neurosci. 2013;263:273-284.
7. Dempster E, Viana J, Pidsley R, Mill J. Epigenetic studies of schizophrenia: progress, predicaments, and promises for the future. Schizophr Bull. 2013;39:11-16.
8. Cisler JM, James GA, Tripathi S, et al. Differential functional connectivity within an emotion regulation neural network among individuals resilient and susceptible to the depressogenic effects of early life stress. Psychol Med. 2013;43:507-518.
9. Sequeira A, Klempan T, Canetti L, et al. Patterns of gene expression in the limbic system of suicides with and without major depression. Mol Psychiatry. 2007;12:640-655.
10. Duman RS, Aghajanian GK. Synaptic dysfunction in depression: potential therapeutic targets. Science. 2012;338:68-72.
11. McEwen BS. Protection and damage from acute and chronic stress: allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Ann NY Acad Sci. 2004;1032:1-7.
12. Ressler KJ, Mayberg HS. Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic. Nat Neurosci. 2007;10:1116-1124.
13. Jenuwein T, Allis CD. Translating the histone code. Science. 2001;293:1074-1080.
14. Strahl BD, Allis CD. The language of covalent histone modifications. Nature. 2000;403:41-45.
15. Klose RJ, Bird AP. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci. 2006;31:89-97.
16. Maunakea AK, Nagarajan RP, Bilenky M, et al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature. 2010;466:253-257.
17. Kriaucionis S, Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science. 2009;324:929- 930.
18. Tahiliani M, Koh KP, Shen Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 2009;324:930-935.
19. 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. 2005;79:734-746.
20. Ma DK, Guo JU, Ming GL, Song H. DNA excision repair proteins and Gadd45 as molecular players for active DNA demethylation. Cell Cycle. 2009;8:1526-1531.
21. Aapola U, Kawasaki K, Scott HS, et al. Isolation and initial characterization of a novel zinc finger gene, DNMT3L, on 21q22.3, related to the cytosine-5-methyltransferase 3 gene family. Genomics. 2000;65:293-298.
22. Berton O, McClung CA, Dileone RJ, et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science. 2006;311:864-868.
23. Wallace DL, Han MH, Graham DL, et al. CREB regulation of nucleus accumbens excitability mediates social isolation-induced behavioral deficits. Nat Neurosci. 2009;12:200-209.
24. Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci. 2006;9:519-525.
25. Covington HE, Maze I, LaPlant QC, et al. Antidepressant actions of histone deacetylase inhibitors. J Neurosci. 2009;29:11451-11460.
26. Schroeder FA, Lin CL, Crusio WE, Akbarian S. Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse. Biol Psychiatry. 2007;62:55-64.
27. Semba J, Kuroda Y, Takahashi R. Potential antidepressant properties of subchronic GABA transaminase inhibitors in the forced swimming test in mice. Neuropsychobiology. 1989;21:152-156.
28. Weaver IC, Cervoni N, Champagne FA, et al. Epigenetic programming by maternal behavior. Nat Neurosci. 2004;7:847-854.
29. Yamawaki Y, Fuchikami M, Morinobu S, Segawa M, Matsumoto T, Yamawaki, S. Antidepressant-like effect of sodium butyrate (HDAC inhibitor) and its molecular mechanism of action in the rat hippocampus. World J Biol Psychiatry. 2012;13:458-467.
30. 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-HT(1A) receptors. Behav Brain Res. 2009;196:200- 206.
31. Uchida S, Hara K, Kobayashi A, et al. Epigenetic status of Gdnf in the ventral striatum determines susceptibility and adaptation to daily stressful events. Neuron. 2011;69:359-372.
32. Renthal W, Maze I, Krishnan V, et al. Histone Deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron. 2007;56:517-529.
33. Covington HE, Maze I, Sun H, et al. A role for repressive histone methylation in cocaine-induced vulnerability to stress. Neuron. 2011;71:656- 670.
34. Hollis F, Duclot F, Gunjan A, Kabbaj, M. Individual differences in the effect of social defeat on anhedonia and histone acetylation in the rat hippocampus. Horm Behav. 2011;59:331-337.
35. Tsankova NM, Kumar A, Nestler EJ. Histone modifications at gene promoter regions in rat hippocampus after acute and chronic electroconvulsive seizures. J Neurosci. 2004;24:5603-5610.
36. Covington HE 3RD, Vialou VF, Laplant Q, Ohnishi YN, Nestler EJ. Hippocampal-dependent antidepressant-like activity of histone deacetylase inhibition. Neurosci Lett. 2011;493:122-126.
37. Sterrenburg L, Gaszner B, Boerrigter J, et al. Chronic stress induces sex-specific alterations in methylation and expression of corticotropinreleasing factor gene in the rat. PLoS One. 2011;6:e28128.
38. Hollis F, Wang H, Dietz D, Gunjan A, Kabbaj M. The effects of repeated social defeat on long-term depressive-like behavior and short-term histone modifications in the hippocampus in male Sprague-Dawley rats. Psychopharmacology. 2010;211:69-77.
39. Hinwood M, Tynan RJ, Day TA, Walker FR. Repeated social defeat selectively increases dFosB expression and histone H3 acetylation in the infralimbic medial prefrontal cortex. Cereb Cortex. 2011;21:262-271.
40. Kenworthy CA, Sengupta A, Luz SM, et al. Social defeat induces changes in histone acetylation and expression of histone modifying enzymes in the ventral hippocampus, prefrontal cortex, and dorsal raphe nucleus. Neuroscience. 2014;264:88-98.
41. Robison AJ, Vialou V, Sun HS, et al. Fluoxetine epigenetically alters the CaMKIIa promoter in nucleus accumbens to regulate ?FosB binding and antidepressant effects. Neuropsychopharmacology. 2014;39:1178-1186.
42. Wilkinson MB, Xiao G, Kumar A, et al. Imipramine treatment and resiliency exhibit similar chromatin regulation in the mouse nucleus accumbens in depression models. J Neurosci. 2009;29:7820-7832.
43. Golden SA, Christoffel DJ, Heshmati M, et al. Epigenetic regulation of RAC1 induces synaptic remodeling in stress disorders and depression. Nat Med. 2013;19:337-344.
44. Hunter RG, McCarthy KJ, Milne TA, Pfaff DW, Mcewen BS. Regulation of hippocampal H3 histone methylation by acute and chronic stress. Proc Natl Acad Sci U S A. 2009;106:20912-20917.
45. Hunter RG, Murakami G, Dewell S, et al. Acute stress and hippocampal histone H3 lysine 9 trimethylation, a retrotransposon silencing response. Proc Natl Acad Sci U S A. 2012;109:17657-17662.
46. Jiang Y, Matevossian A, Huang HS, Straubhaar J, Akbarian S. Isolation of neuronal chromatin from brain tissue. BMC Neurosci. 2008;9:42.
47. Cruceanu C, Alda M, Nagy C, Freemantle E, Rouleau GA, Turecki G. H3K4 tri-methylation in synapsin genes leads to different expression patterns in bipolar disorder and major depression. Int J Neuropsychopharmacol. 2013;16:289-299.
48. Fiori LM, Gross JA, Turecki G. Effects of histone modifications on increased expression of polyamine biosynthetic genes in suicide. Int J Neuropsychopharmacol. 2012;15:1161-1166.
49. Ernst C, Chen ES, Turecki G. Histone methylation and decreased expression of TrkB.T1 in orbital frontal cortex of suicide completers. Mol Psychiatry. 2009;14:830-832.
50. Ernst C, Deleva V, Deng X, et al. Alternative splicing, methylation state, and expression profile of tropomyosin-related kinase B in the frontal cortex of suicide completers. Arch Gen Psychiatry. 2009;66:22-32.
51. Razzoli M, Domenici E, Carboni L, et al. A role for BDNF/TrkB signaling in behavioral and physiological consequences of social defeat stress. Genes Brain Behav. 2011;10:424-433.
52. Chen ES, Ernst C, Turecki G. The epigenetic effects of antidepressant treatment on human prefrontal cortex BDNF expression. Int J Neuropsychopharmacol. 2011;14:427-429.
53. Lopez JP, Mamdani F, Labonte B, et al. Epigenetic regulation of BDNF expression according to antidepressant response. Mol Psychiatry. 2013;18:398-399.
54. LaPlant Q, Vialou V, Covington HE, et al. Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nature Neuroscience. 2010;13:1137-1143.
55. Elliott EE, Ezra-Nevo GG, Regev LL, Neufeld-Cohen AA, Chen AA. Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice. Nat Neurosci. 2010;13:1351-1353.
56. Fyffe SL, Neul JL, Samaco RC, et al. Deletion of Mecp2 in Sim1-expressing neurons reveals a critical role for MeCP2 in feeding behavior, aggression, and the response to stress. Neuron. 2008;59:947-958.
57. Mill J, Tang T, Kaminsky Z, et al. Epigenomic profiling reveals DNAmethylation changes associated with major psychosis. Am J Hum Genet. 2008;82:696-711.
58. Ladd-Acosta C, Pevsner J, Sabunciyan S, et al. DNA methylation signatures within the human brain. Am J Hum Genet. 2007;81:1304-1315.
59. Deaton AM, Webb S, Kerr AR, et al. Cell type-specific DNA methylation at intragenic CpG islands in the immune system. Genome Res. 2011;21:1074-1086.
60. Iwamoto K, Bundo M, Ueda J, et al. Neurons show distinctive DNA methylation profile and higher interindividual variations compared with non-neurons. Genome Res. 2011;21:688-696.
61. Heim C, Nemeroff CB. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry. 2001;49:1023-1039.
62. Holmes SJ, Robins LN. The influence of childhood disciplinary experience on the development of alcoholism and depression. J Child Psychol Psychiatry. 1987;28:399-415.
63. Enoch MA. The role of early life stress as a predictor for alcohol and drug dependence. Psychopharmacology. 2011;214:17-31.
64. Riggs S, Alario AJ. Adolescent substance use and the role of the primary care provider. R I Med J. 1990;73:253-257.
65. Meaney MJ. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci. 2001;24:1161-1192.
66. Matrisciano F, Tueting P, Dalal I, et al. Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice. Neuropharmacology. 2013;68:184- 194.
67. 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;45:488-498.
68. Blaze J, Roth TL. Exposure to caregiver maltreatment alters expression levels of epigenetic regulators in the medial prefrontal cortex. Int J Dev Neurosci. 2013;31:804-810.
69. Xie L, Korkmaz KS, Braun K, Bock J. Early life stress-induced histone acetylations correlate with activation of the synaptic plasticity genes Arc and Egr1 in the mouse hippocampus. J Neurochem. 2013;125:457-464.
70. Bagot RC, Zhang TY, Wen X, et al. Variations in postnatal maternal care and the epigenetic regulation of metabotropic glutamate receptor 1 expression and hippocampal function in the rat. Proc Natl Acad Sci U S A. 2012;109:17200-17207.
71. McGowan PO, Suderman M, Sasaki A, et al. Broad epigenetic signature of maternal care in the brain of adult rats. PLoS One. 2011;6:e14739.
72. Zhang TY, Hellstrom IC, Bagot RC, Wen X, Diorio J, Meaney MJ. Maternal care and DNA methylation of a glutamic acid decarboxylase 1 promoter in rat hippocampus. J Neurosci. 2010;30:13130-13137.
73. Weaver IC, Meaney MJ, Szyf M. Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc Natl Acad Sci U S A. 2006;103:3480- 3485.
74. Gitau R, Cameron A, Fisk NM, Glover V. Fetal exposure to maternal cortisol. Lancet. 1998;352:707-708.
75. Jensen Peña C, Monk C, Champagne FA. Epigenetic effects of prenatal stress on 11ß-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain. PLoS One. 2012;7:e39791-e39791.
76. Mairesse J, Lesage J, Breton C, et al. Maternal stress alters endocrine function of the feto-placental unit in rats. Am J Physiol Endo Metab. 2007;292:E1526-E1533.
77. O'Donnell KJ, Bugge Jensen A, Freeman L, Khalife N, O'Connor TG, Glover V. Maternal prenatal anxiety and downregulation of placental 11ß-HSD2. Psychoneuroendocrinology. 2012;37:818-826.
78. Holmes MC, Abrahamsen CT, French KL, Paterson JM, Mullins JJ, Seckl JR. The mother or the fetus? 11beta-hydroxysteroid dehydrogenase type 2 null mice provide evidence for direct fetal programming of behavior by endogenous glucocorticoids. J Neurosci. 2006;26:3840-3844.
79. Welberg LA, Seckl JR, Holmes MC. Inhibition of 11beta-hydroxysteroid dehydrogenase, the foeto-placental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxietylike behaviour in the offspring. Eur J Neurosci. 2000;12:1047-1054.
80. Mueller BR, Bale TL. Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci. 2008;28:9055-9065.
81. Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics. 2008;3:97-106.
82. Hompes T, Izzi B, Gellens E, et al. Investigating the influence of maternal cortisol and emotional state during pregnancy on the DNA methylation status of the glucocorticoid receptor gene (NR3C1) promoter region in cord blood. J Psychiatr Res. 2013;47:880-891.
83. Radtke KM, Ruf M, Gunter HM, et al. Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Transl Psychiatry. 2011;1:e21.
84. Devlin AM, Brain U, Austin J, Oberlander TF. Prenatal exposure to maternal depressed mood and the MTHFR C677T variant affect SLC6A4 methylation in infants at birth. PLoS One. 2010;5:e12201.
85. Schroeder J, Smith A, Brennan P, et al. DNA methylation in neonates born to women receiving psychiatric care. Epigenetics. 2012;7:409-414.
86. Suderman M, McGowan PO, Sasaki A, et al. Conserved epigenetic sensitivity to early life experience in the rat and human hippocampus. Proc Natl Acad Sci U S A. 2012;109:17266-17272.
87. Peña CJ, Neugut YD, Champagne FA. Developmental timing of the effects of maternal care on gene expression and epigenetic regulation of hormone receptor levels in female rats. Endocrinology. 2013;154:4340- 4351.
88. Labonte B, Yerko V, Gross J, et al. Differential glucocorticoid receptor exon 1(B), 1(C), and 1(H) expression and methylation in suicide completers with a history of childhood abuse. Biol Psychiatry. 2012;72:41-48.
89. McGowan PO, Sasaki A, D'Alessio AC, et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci. 2009;12:342-348.
90. Perroud N, Paoloni-Giacobino A, Prada P, et al. Increased methylation of glucocorticoid receptor gene (NR3C1) in adults with a history of childhood maltreatment: a link with the severity and type of trauma. Transl Psychiatry. 2011;1:e59.
91. Tyrka AR, Price LH, Marsit C, Walters OC, Carpenter LL. Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: preliminary findings in healthy adults. PLoS One. 2012;7:e30148.
92. Alt SR, Turner JD, Klok MD, et al. Differential expression of glucocorticoid receptor transcripts in major depressive disorder is not epigenetically programmed. Psychoneuroendocrinology. 2010;35:544-556.
93. Guidotti A, Auta J, Davis JM, et al. Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch Gen Psychiatry. 2000;57:1061-1069.
94. Veldic M, Caruncho HJ, Liu WS, et al. DNA-methyltransferase 1 mRNA is selectively overexpressed in telencephalic GABAergic interneurons of schizophrenia brains. Proc Natl Acad Sci U S A. 2004;101:348-353.
95. Kundakovic M, Chen Y, Costa E, Grayson DR. DNA methyltransferase inhibitors coordinately induce expression of the human reelin and glutamic acid decarboxylase 67 genes. Mol Pharmacol. 2007;71:644-653.
96. Grayson DR, Jia X, Chen Y, et al. Reelin promoter hypermethylation in schizophrenia. Proc Natl Acad Sci U S A. 2005;102:9341-9346.
97. Tamura Y, Kunugi H, Ohashi J, Hohjoh H. Epigenetic aberration of the human REELIN gene in psychiatric disorders. Mol Psychiatry. 2007;12:593-600.
98. Poulter MO, Du L, Weaver IC, et al. GABAA receptor promoter hypermethylation in suicide brain: implications for the involvement of epigenetic processes. Biol Psychiatry. 2008;64:645-652.
99. Murgatroyd C, Patchev AV, Wu Y, et al. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci. 2009;12:1559-1566.
100. Niwa M, Jaaro-Peled H, Tankou S, et al. Adolescent stress-induced epigenetic control of dopaminergic neurons via glucocorticoids. Science. 2013;339:335-339.
101. Labonte B, Suderman M, Maussion G, et al. Genome-wide epigenetic regulation by early-life trauma. Arch Gen Psychiatry. 2012;69:722-731.
102. Uddin M, Aiello AE, Wildman DE, et al. Epigenetic and immune function profiles associated with posttraumatic stress disorder. Proc Natl Acad Sci U S A. 2010;107:9470-9475.
103. Roth TL, Lubin FD, Funk AJ, Sweatt JD. Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol Psychiatry. 2009;65:760-769.
104. Roth TL, Zoladz PR, Sweatt JD, Diamond DM. Epigenetic modification of hippocampal Bdnf DNA in adult rats in an animal model of posttraumatic stress disorder. J Psychiatr Res. 2011;45:919-926.
105. Sun H, Kennedy PJ, Nestler EJ. Epigenetics of the depressed brain: role of histone acetylation and methylation. Neuropsychopharmacology. 2013;38:124-137.