Epigenetic alterations related to early-life stressful events

Acta Neuropsychiatrica

Volumn 24, Issue 5, 2012, Pages 255-265

  Ventura Junca, Raúl ^a,b   Herrera, Luisa M ^b  

^a UNIVERSIDAD DE LOS ANDES   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

Author keywords

behaviour; early stress; epigenetic; HPA; methylation

Indexed keywords

ARGIPRESSIN; BRAIN DERIVED NEUROTROPHIC FACTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FK 506 BINDING PROTEIN; GLUCOCORTICOID RECEPTOR; HISTONE; HORMONE RECEPTOR STIMULATING AGENT; METHYL CPG BINDING PROTEIN 2; MICRORNA; MINERALOCORTICOID RECEPTOR; NELIVAPTAN; SEROTONIN;

ABNORMAL BEHAVIOR; DISEASE ASSOCIATION; DNA METHYLATION; EARLY LIFE STRESS; EMPIRICAL RESEARCH; EPIGENETICS; GENE EXPRESSION; GENETIC REGULATION; HUMAN; LIFE EVENT; NERVE CELL PLASTICITY; NEUROANATOMY; NEUROTRANSMISSION; NONHUMAN; REVIEW;

EID: 84866523624     PISSN: 09242708     EISSN: 16015215     Source Type: Journal    
DOI: 10.1111/j.1601-5215.2012.00683.x     Document Type: Review

References (139)

1. Ramiro LS, Madrid BJ, Brown DW,. Adverse childhood experiences (ACE) and health-risk behaviors among adults in a developing country setting. Child Abuse Negl 2010; 34: 842-855.
2. Van Der Vegt EJ, Tieman W, Van Der Ende J, Ferdinand RF, Verhulst FC, Tiemeier H,. Impact of early childhood adversities on adult psychiatric disorders: a study of international adoptees. Soc Psychiatry Psychiatr Epidemiol 2009; 44: 724-731.
3. Mclaughlin KA, Green JG, Gruber MJ, Sampson NA, Zaslavsky AM, Kessler RC,. Childhood adversities and adult psychopathology in the National Comorbidity Survey Replication (NCS-R) III: associations with functional impairment related to DSM-IV disorders. Psychol Med 2010; 40: 847-859.
4. Alloy LB, Abramson LY, Smith JM, Gibb BE, Neeren AM,. Role of parenting and maltreatment histories in unipolar and bipolar mood disorders: mediation by cognitive vulnerability to depression. Clin Child Fam Psychol Rev 2006; 9: 23-64.
5. Kessler RC, Davis CG, Kendler KS,. Childhood adversity and adult psychiatric disorder in the US National Comorbidity Survey. Psychol Med 1997; 27: 1101-1119.
6. Afifi TO, Mather A, Boman J, et al. Childhood adversity and personality disorders: Results from a nationally representative population-based study. J Psychiatr Res 2011; 45: 814-822.
7. Kessler RC, Berglund P, Demler O, Jin R, Merikangas KR, Walters EE,. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 2005; 62: 593-602.
8. Belsky J, Steinberg L, Houts RM, Halpern-Felsher BL,. The development of reproductive strategy in females: early maternal harshness → earlier menarche → increased sexual risk taking. Dev Psychol 2010; 46: 120-128.
9. Beck AT,. The evolution of the cognitive model of depression and its neurobiological correlates. Am J Psychiatry 2008; 165: 969-977.
10. WHO. Child Maltreatment. World Health Organization Fact Sheet No. 150, 2010.
11. Herman JP, Ostrander MM, Mueller NK, Figueiredo H,. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 2005; 29: 1201-1213.
12. Penza KM, Heim C, Nemeroff CB,. Neurobiological effects of childhood abuse: implications for the pathophysiology of depression and anxiety. Arch Womens Ment Health 2003; 6: 15-22.
13. Jackowski A, Perera TD, Abdallah CG, et al. Early-life stress, corpus callosum development, hippocampal volumetrics, and anxious behavior in male nonhuman primates. Psychiatry Res 2011; 192: 37-44.
14. Vythilingam M, Heim C, Newport J, et al. Childhood trauma associated with smaller hippocampal volume in women with major depression. Am J Psychiatry 2002; 159: 2072-2080.
15. Driessen M, Herrmann J, Stahl K, et al. Magnetic resonance imaging volumes of the hippocampus and the amygdala in women with borderline personality disorder and early traumatization. Arch Gen Psychiatry 2000; 57: 1115-1122.
16. Mirescu C, Gould E,. Stress and adult neurogenesis. Hippocampus 2006; 16: 233-238.
17. Mcewen BS,. Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 2005; 54: 20-23.
18. Liston C, Miller MM, Goldwater DS, et al. Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 2006; 26: 7870-7874.
19. Radley JJ, Sisti HM, Hao J, et al. Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 2004; 125: 1-6.
20. Mitra R, Jadhav S, Mcewen BS, Vyas A, Chattarji S,. Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc Natl Acad Sci USA 2005; 102: 9371-9376.
21. Vyas A, Jadhav S, Chattarji S,. Prolonged behavioral stress enhances synaptic connectivity in the basolateral amygdala. Neuroscience 2006; 143: 387-393.
22. Woon FL, Hedges DW,. Hippocampal and amygdala volumes in children and adults with childhood maltreatment-related posttraumatic stress disorder: a meta-analysis. Hippocampus 2008; 18: 729-736.
23. Pruessner JC, Baldwin MW, Dedovic K, et al. Self-esteem, locus of control, hippocampal volume, and cortisol regulation in young and old adulthood. Neuroimage 2005; 28: 815-826.
24. Wilner AP, De Varennes B, Gregoire PA, Lupien S, Pruessner JC,. Glucocorticoids and hippocampal atrophy after heart transplantation. Ann Thorac Surg 2002; 73: 1965-1967.
25. De Bellis MD, Keshavan MS, Shifflett H, et al. Brain structures in pediatric maltreatment-related posttraumatic stress disorder: a sociodemographically matched study. Biol Psychiatry 2002; 52: 1066-1078.
26. Nemeroff CB, Vale WW,. The neurobiology of depression: inroads to treatment and new drug discovery. J Clin Psychiatry 2005; 66 (Suppl. 7): 5-13.
27. Engelmann M, Landgraf R, Wotjak CT,. The hypothalamic-neurohypophysial system regulates the hypothalamic-pituitary-adrenal axis under stress: an old concept revisited. Front Neuroendocrinol 2004; 25: 132-149.
28. Aguilera G, Rabadan-Diehl C,. Vasopressinergic regulation of the hypothalamic-pituitary-adrenal axis: implications for stress adaptation. Regul Pept 2000; 96: 23-29.
29. Sandi C,. Stress, cognitive impairment and cell adhesion molecules. Nature reviews. 2004; 5: 917-930.
30. Charmandari E, Tsigos C, Chrousos G,. Endocrinology of the stress response. Annu Rev Physiol 2005; 67: 259-284.
31. Rentesi G, Antoniou K, Marselos M, Fotopoulos A, Alboycharali J, Konstandi M,. Long-term consequences of early maternal deprivation in serotonergic activity and HPA function in adult rat. Neurosci Lett 2010; 480: 7-11.
32. Heim C, Mletzko T, Purselle D, Musselman DL, Nemeroff CB,. The dexamethasone/corticotropin-releasing factor test in men with major depression: role of childhood trauma. Biol Psychiatry 2008; 63: 398-405.
33. Weiss EL, Longhurst JG, Mazure CM,. Childhood sexual abuse as a risk factor for depression in women: psychosocial and neurobiological correlates. Am J Psychiatry 1999; 156: 816-828.
34. Shea A, Walsh C, Macmillan H, Steiner M,. Child maltreatment and HPA axis dysregulation: relationship to major depressive disorder and post traumatic stress disorder in females. Psychoneuroendocrinology 2005; 30: 162-178.
35. Heim C, Plotsky PM, Nemeroff CB,. Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology 2004; 29: 641-648.
36. Rasmusson AM, Lipschitz DS, Wang S, et al. Increased pituitary and adrenal reactivity in premenopausal women with posttraumatic stress disorder. Biol Psychiatry 2001; 50: 965-977.
37. Yehuda R, Bierer LM, Schmeidler J, Aferiat DH, Breslau I, Dolan S,. Low cortisol and risk for PTSD in adult offspring of holocaust survivors. Am J Psychiatry 2000; 157: 1252-1259.
38. Holsboer F,. The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 2000; 23: 477-501.
39. Clarke AS, Wittwer DJ, Abbott DH, Schneider ML,. Long-term effects of prenatal stress on HPA axis activity in juvenile rhesus monkeys. Dev Psychobiol 1994; 27: 257-269.
40. Liu D, Diorio J, Tannenbaum B, et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science (New York, NY) 1997; 277: 1659-1662.
41. Sterlemann V, Ganea K, Liebl C, et al. Long-term behavioral and neuroendocrine alterations following chronic social stress in mice: implications for stress-related disorders. Horm Behav 2008; 53: 386-394.
42. Pryce CR,. Postnatal ontogeny of expression of the corticosteroid receptor genes in mammalian brains: Inter-species and intra-species differences. Brain Res Rev 2008; 57: 596-605.
43. Ridder S, Chourbaji S, Hellweg R, et al. Mice with genetically altered glucocorticoid receptor expression show altered sensitivity for stress-induced depressive reactions. J Neurosci 2005; 25: 6243-6250.
44. Zhang TY, Meaney MJ,. Epigenetics and the environmental regulation of the genome and its function. Annu Rev Psychol 2010; 61 (439-466): C431-433.
45. Caiafa P, Zampieri M,. DNA methylation and chromatin structure: the puzzling CpG islands. J Cell Biochem 2005; 94: 257-265.
46. Bonasio R, Tu S, Reinberg D,. Molecular signals of epigenetic states. Science 2010; 330: 612-616.
47. Hoffmann A,., Spengler D,. Neuroscience: DNA memories of early social life, 2012.
48. Szyf M,. DNA methylation and demethylation probed by small molecules. Biochim Biophys Acta 2010; 1799: 750-759.
49. Lee JY, Lee TH,. Effects of histone acetylation and CpG methylation on the structure of nucleosomes. Biochim Biophys Acta 2012; 1824: 974-982.
50. Bannister AJ, Kouzarides T,. Regulation of chromatin by histone modifications. Cell Res 2011; 21: 381-395.
51. Margueron R, Trojer P, Reinberg D,. The key to development: interpreting the histone code? Curr Opin Genet Dev 2005; 15: 163-176.
52. Lessard JA, Crabtree GR,. Chromatin regulatory mechanisms in pluripotency. Annu Rev Cell Dev Biol 2010; 26: 503-532.
53. Racki LR, Narlikar GJ,. ATP-dependent chromatin remodeling enzymes: two heads are not better, just different. Curr Opin Genet Dev 2008; 18: 137-144.
54. Hota SK, Bartholomew B,. Diversity of operation in ATP-dependent chromatin remodelers. Biochim Biophys Acta 2011; 1809: 476-487.
55. Erdel F, Krug J, Langst G, Rippe K,. Targeting chromatin remodelers: signals and search mechanisms. Biochim Biophys Acta 2011; 1809: 497-508.
56. Magistri M, Faghihi MA, St Laurent G 3rd, Wahlestedt C., Regulation of chromatin structure by long noncoding RNAs: focus on natural antisense transcripts. Trends Genet 2012; 28: 389-396.
57. Qureshi IA, Mehler MF., Epigenetic mechanisms underlying human epileptic disorders and the process of epileptogenesis. Neurobiol Disease 2010; 39: 53-60.
58. Davis-Dusenbery BN, Hata A,. Mechanisms of control of microRNA biogenesis. J Biochem 2010; 148: 381-392.
59. Saxena A, Carninci P,. Long non-coding RNA modifies chromatin: epigenetic silencing by long non-coding RNAs. BioEssays: news and reviews in molecular, cellular and developmental biology. 2011; 33: 830-839.
60. Aalto AP, Pasquinelli AE,. Small non-coding RNAs mount a silent revolution in gene expression. Curr Opin Cell Biol 2012; 24: 333-340.
61. Shukla GC, Singh J, Barik S,. MicroRNAs: processing, maturation, target recognition and regulatory functions. Molecular Cell Pharmacol 2011; 3: 83-92.
62. Schratt G,. Fine-tuning neural gene expression with microRNAs. Curr Opin Neurobiol 2009; 19: 213-219.
63. Weaver IC,. Shaping adult phenotypes through early life environments. Birth Defects Res C Embryo Today 2009; 87: 314-326.
64. Lenroot RK, Giedd JN,. Annual research review: developmental considerations of gene by environment interactions. J Child Psychol Psychiatry 2011; 52: 429-441.
65. Anda RF, Felitti VJ, Bremner JD, et al. The enduring effects of abuse and related adverse experiences in childhood. A convergence of evidence from neurobiology and epidemiology. Eur Arch Psychiatry Clin Neurosci 2006; 256: 174-186.
66. Bradley RG, Binder EB, Epstein MP, et al. Influence of child abuse on adult depression: moderation by the corticotropin-releasing hormone receptor gene. Arch Gen Psychiatry 2008; 65: 190-200.
67. Chapman DP, Whitfield CL, Felitti VJ, Dube SR, Edwards VJ, Anda RF,. Adverse childhood experiences and the risk of depressive disorders in adulthood. J Affect Disord 2004; 82: 217-225.
68. Szyf M,. The early life environment and the epigenome. Biochim Biophys Acta 2009; 1790: 878-885.
69. Meaney MJ, Szyf M, Seckl JR,. Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Mol Med 2007; 13: 269-277.
70. Murgatroyd C, Wu Y, Bockmuhl Y, Spengler D,. Genes learn from stress: how infantile trauma programs us for depression. Epigenetics 2010; 5: 194-199.
71. Champagne FA,. Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 2008; 29: 386-397.
72. Mcleod J, Sinal CJ, Perrot-Sinal TS,. Evidence for non-genomic transmission of ecological information via maternal behavior in female rats. Genes Brain Behav 2007; 6: 19-29.
73. Franklin TB, Russig H, Weiss IC, et al. Epigenetic transmission of the impact of early stress across generations. Biol Psychiatry 2010; 68: 408-415.
74. Fernandez-Guasti A, Fiedler JL, Herrera L, Handa RJ,. Sex, stress, and mood disorders: at the intersection of adrenal and gonadal hormones. Horm Metab Res 2012; 44: 607-618.
75. Weaver IC, Cervoni N, Champagne FA, et al. Epigenetic programming by maternal behavior. Nat Neurosci 2004; 7: 847-854.
76. Murgatroyd C, Spengler D,. Epigenetics of early child development. Front Psychiatry/Front Res Found 2011; 2: 16.
77. Uchida S, Hara K, Kobayashi A, et al. Early life stress enhances behavioral vulnerability to stress through the activation of REST4-mediated gene transcription in the medial prefrontal cortex of rodents. J Neurosci 2010; 30: 15007-15018.
78. 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.
79. Tognini P, Pizzorusso T,. MicroRNA212/132 family: molecular transducer of neuronal function and plasticity. Int J Biochem Cell Biol 2012; 44: 6-10.
80. Weaver IC,. Epigenetic effects of glucocorticoids. Semin Fetal Neonatal Med 2009; 14: 143-150.
81. Maestripieri D,. Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys. Proc Natl Acad Sci USA 2005; 102: 9726-9729.
82. Zhang TY, Bagot R, Parent C, et al. Maternal programming of defensive responses through sustained effects on gene expression. Biol Psychol 2006; 73: 72-89.
83. Bagot RC, Van Hasselt FN, Champagne DL, Meaney MJ, Krugers HJ, Joels M,. Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus. Neurobiol Learn Mem 2009; 92: 292-300.
84. Szyf M, Weaver IC, Champagne FA, Diorio J, Meaney MJ,. Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Front Neuroendocrinol 2005; 26: 139-162.
85. Weaver IC, D'Alessio AC, Brown SE, et al. The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: altering epigenetic marks by immediate-early genes. J Neurosci 2007; 27: 1756-1768.
86. Cervoni N, Szyf M,. Demethylase activity is directed by histone acetylation. J Biol Chem 2001; 276: 40778-40787.
87. 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.
88. Alt SR, Turner JD, Klok MD, et al. Differential expression of glucocorticoid receptor transcripts in major depressive disorder is not epigenetically programmed. Psychoneuroendocrinology 2009; 35: 544-556.
89. Binder EB, Salyakina D, Lichtner P, et al. Polymorphisms in FKBP5 are associated with increased recurrence of depressive episodes and rapid response to antidepressant treatment. Nat Genet 2004; 36: 1319-1325.
90. Willour VL, Chen H, Toolan J, et al. Family-based association of FKBP5 in bipolar disorder. Mol Psychiatry 2009; 14: 261-268.
91. Binder EB, Bradley RG, Liu W, et al. Association of FKBP5 polymorphisms and childhood abuse with risk of posttraumatic stress disorder symptoms in adults. JAMA 2008; 299: 1291-1305.
92. Brent D, Melhem N, Ferrell R, et al. Association of FKBP5 polymorphisms with suicidal events in the Treatment of Resistant Depression in Adolescents (TORDIA) study. Am J Psychiatry 2010; 167: 190-197.
93. Supriyanto I, Sasada T, Fukutake M, et al. Association of FKBP5 gene haplotypes with completed suicide in the Japanese population. Prog Neuropsychopharmacol Biol Psychiatry 2011; 35: 252-256.
94. Luijk MP, Velders FP, Tharner A, et al. FKBP5 and resistant attachment predict cortisol reactivity in infants: gene-environment interaction. Psychoneuroendocrinology 2010; 35: 1454-1461.
95. Shibuya N, Suzuki A, Sadahiro R, et al. Association study between a functional polymorphism of FK506-binding protein 51 (FKBP5) gene and personality traits in healthy subjects. Neurosci Lett 2010; 485: 194-197.
96. Hartmann J, Wagner KV, Liebl C, et al. The involvement of FK506-binding protein 51 (FKBP5) in the behavioral and neuroendocrine effects of chronic social defeat stress. Neuropharmacology 2012; 62: 332-339.
97. Lee RS, Tamashiro KL, Yang X, et al. Chronic corticosterone exposure increases expression and decreases deoxyribonucleic acid methylation of Fkbp5 in mice. Endocrinology 2010; 151: 4332-4343.
98. 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.
99. Lopez-Leon S, Janssens AC, Gonzalez-Zuloeta Ladd AM, et al. Meta-analyses of genetic studies on major depressive disorder. Mol Psychiatry 2007; 13: 772-785.
100. Sarapas C, Cai G, Bierer LM, et al. Genetic markers for PTSD risk and resilience among survivors of the World Trade Center attacks. Dis Markers 2011; 30: 101-110.
101. Mcewen BS, Alves SE,. Estrogen actions in the central nervous system. Endocr Rev 1999; 20: 279-307.
102. Weiser MJ, Foradori CD, Handa RJ,. Estrogen receptor beta in the brain: from form to function. Brain Res Rev 2008; 57: 309-320.
103. Bodo C, Rissman EF,. New roles for estrogen receptor beta in behavior and neuroendocrinology. Front Neuroendocrinol 2006; 27: 217-232.
104. Kirschbaum C, Kudielka BM, Gaab J, Schommer NC, Hellhammer DH,. Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosom Med 1999; 61: 154-162.
105. Kumsta R, Entringer S, Koper JW, Van Rossum EF, Hellhammer DH, Wust S,. Sex specific associations between common glucocorticoid receptor gene variants and hypothalamus-pituitary-adrenal axis responses to psychosocial stress. Biol Psychiatry 2007; 62: 863-869.
106. Cameron NM, Shahrokh D, Del Corpo A, et al. Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care. J Neuroendocrinol 2008; 20: 795-801.
107. Caspi A, Sugden K, Moffitt TE, et al. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 2003; 301: 386-389.
108. Lesch KP, Bengel D, Heils A, et al. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 1996; 274: 1527-1531.
109. Kendler KS, Kuhn JW, Vittum J, Prescott CA, Riley B,. The interaction of stressful life events and a serotonin transporter polymorphism in the prediction of episodes of major depression: a replication. Arch Gen Psychiatry 2005; 62: 529-535.
110. Murphy DL, Moya PR,. Human serotonin transporter gene (SLC6A4) variants: their contributions to understanding pharmacogenomic and other functional GxG and GxE differences in health and disease. Curr Opin Pharmacol 2011; 11: 3-10.
111. Alessandro S, Kato M,. The serotonin transporter gene and effectiveness of SSRIs. Expert Rev Neurother 2008; 8: 111-120.
112. Karg K, Burmeister M, Shedden K, Sen S,. The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited: evidence of genetic moderation. Arch Gen Psychiatry 2011; 68: 444-454.
113. Philibert R, Madan A, Andersen A, Cadoret R, Packer H, Sandhu H,. Serotonin transporter mRNA levels are associated with the methylation of an upstream CpG island. Am J Med Genet B Neuropsychiatr Genet 2007; 144B: 101-105.
114. Van Ijzendoorn MH, Caspers K, Bakermans-Kranenburg MJ, Beach SR, Philibert R,. Methylation matters: interaction between methylation density and serotonin transporter genotype predicts unresolved loss or trauma. Biol Psychiatry 2010; 68: 405-407.
115. Kochanska G, Philibert RA, Barry RA,. Interplay of genes and early mother-child relationship in the development of self-regulation from toddler to preschool age. J Child Psychol Psychiatry 2009; 50: 1331-1338.
116. 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.
117. 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.
118. Russo-Neustadt A,. Brain-derived neurotrophic factor, behavior, and new directions for the treatment of mental disorders. Semin Clin Neuropsychiatry 2003; 8: 109-118.
119. Angelucci F, Brene S, Mathe AA,. BDNF in schizophrenia, depression and corresponding animal models. Mol Psychiatry 2005; 10: 345-352.
120. Colzato LS, Van Der Does AJ, Kouwenhoven C, Elzinga BM, Hommel B,. BDNF Val(66)Met polymorphism is associated with higher anticipatory cortisol stress response, anxiety, and alcohol consumption in healthy adults. Psychoneuroendocrinology 2011; 36: 1562-1569.
121. Karege F, Perret G, Bondolfi G, Schwald M, Bertschy G, Aubry JM,. Decreased serum brain-derived neurotrophic factor levels in major depressed patients. Psychiatry Res 2002; 109: 143-148.
122. Aydemir O, Deveci A, Taneli F,. The effect of chronic antidepressant treatment on serum brain-derived neurotrophic factor levels in depressed patients: a preliminary study. Prog Neuropsychopharmacol Biol Psychiatry 2005; 29: 261-265.
123. Magarinos AM, Mcewen BS, Flugge G, Fuchs E,. Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci 1996; 16: 3534-3540.
124. Murakami S, Imbe H, Morikawa Y, Kubo C, Senba E,. Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly. Neurosci Res 2005; 53: 129-139.
125. Smith MA, Makino S, Kvetnansky R, Post RM,. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci 1995; 15: 1768-1777.
126. Taliaz D, Stall N, Dar DE, Zangen A,. Knockdown of brain-derived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis. Mol Psychiatry 2010; 15: 80-92.
127. Taliaz D, Loya A, Gersner R, Haramati S, Chen A, Zangen A,. Resilience to chronic stress is mediated by hippocampal brain-derived neurotrophic factor. J Neurosci 2011; 31: 4475-4483.
128. Tapia-Arancibia L, Rage F, Givalois L, Arancibia S,. Physiology of BDNF: focus on hypothalamic function. Front Neuroendocrinol 2004; 25: 77-107.
129. Patapoutian A, Reichardt LF,. Trk receptors: mediators of neurotrophin action. Curr Opin Neurobiol 2001; 11: 272-280.
130. Carlezon WA Jr, Duman RS, Nestler EJ,. The many faces of CREB. Trends Neurosci 2005; 28: 436-445.
131. 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.
132. Roth TL, Sweatt JD,. Epigenetic marking of the BDNF gene by early-life adverse experiences. Horm Behav 2011; 59: 315-320.
133. Lubin FD, Roth TL, Sweatt JD,. Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J Neurosci 2008; 28: 10576-10586.
134. Branchi I, Francia N, Alleva E,. Epigenetic control of neurobehavioural plasticity: the role of neurotrophins. Behav Pharmacol 2004; 15: 353-362.
135. Fumagalli F, Molteni R, Racagni G, Riva MA,. Stress during development: Impact on neuroplasticity and relevance to psychopathology. Prog Neurobiol 2007; 81: 197-217.
136. Lippmann M, Bress A, Nemeroff CB, Plotsky PM, Monteggia LM,. Long-term behavioural and molecular alterations associated with maternal separation in rats. Eur J Neurosci 2007; 25: 3091-3098.
137. Zhang TY, Parent C, Weaver I, Meaney MJ,. Maternal programming of individual differences in defensive responses in the rat. Ann N Y Acad Sci 2004; 1032: 85-103.
138. Balbernie R,. Reactive attachment disorder as an evolutionary adaptation. Attach Hum Dev 2010; 12: 265-281.
139. Crews D,. Epigenetics and its implications for behavioral neuroendocrinology. Front Neuroendocrinol 2008; 29: 344-357.