Long-term effects of early life stress exposure: Role of epigenetic mechanisms

Pharmacological Research

Volumn 109, Issue , 2016, Pages 64-73

  Silberman, Dafne M ^a   Acosta, Gabriela B ^b   Zorrilla Zubilete, María A ^a  

^a Centre de Estudios Farmacologicos y Botanicos   (Argentina)

^b Instituto de Investigaciones Farmacologicas   (Argentina)

Author keywords

BDNF; HDAC inhibitors; HPA axis; Maternal separation; Prenatal stress; Stress response

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 2; BRAIN DERIVED NEUROTROPHIC FACTOR; BUTYRIC ACID; FLUOXETINE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; GLUTAMATE RECEPTOR; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE; OXYTOCIN; VALPROIC ACID; VORINOSTAT;

ALZHEIMER DISEASE; BIPOLAR DISORDER; BRAIN DEVELOPMENT; CHILD ABUSE; CHRONIC STRESS; CORTICOSTEROID RELEASE; DNA METHYLATION; EARLY LIFE STRESS; ENVIRONMENTAL ENRICHMENT; EPIGENETICS; GENE EXPRESSION REGULATION; HISTONE ACETYLATION; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MATERNAL DEPRIVATION; MATERNAL STRESS; MENTAL DISEASE; NONHUMAN; OXIDATIVE STRESS; PERINATAL STRESS; POSTTRAUMATIC STRESS DISORDER; PRENATAL STRESS; PRIORITY JOURNAL; REVIEW; ANIMAL; FEMALE; GENETIC EPIGENESIS; GENETICS; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MENTAL STRESS; PREGNANCY; PRENATAL EXPOSURE;

ANIMALS; EPIGENESIS, GENETIC; FEMALE; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; PITUITARY-ADRENAL SYSTEM; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; STRESS, PSYCHOLOGICAL;

EID: 84971473615     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2015.12.033     Document Type: Review

References (180)

1. E. Llorente, M.L. Brito, P. Machado, and M.C. González Effect of prenatal stress on the hormonal response to acute and chronic stress and on immune parameters in the offspring J. Physiol. Biochem. 58 2002 143 149
2. G. Kay, N. Tarcic, T. Poltyrev, and M. Weinstock Prenatal stress depresses immune function in rats Physiol. Behav. 63 1998 397 402
3. C.C. Vanbesien-Mailliot, I. Wolowczuk, J. Mairesse, O. Viltart, M. Delacre, J. Khalife, M.C. Chartier-Harlin, and S. Maccari Prentral stress has pro-inflammatory consequences on the immune system in adult rats Psychoneuroendocrinology 32 2007 2007 114 124
4. S. Maccari, and S. Morley-Fletcher Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations Psychoneuroendocrinology 32 Suppl. 1 2007 S10 15
5. Y. Diz-Chaves, M. Astiz, M.J. Bellini, and L.M. Garcia-Segura Prenatal stress increases the expression of proinflammatory cytokines and exacerbates the inflammatory response to LPS in the hippocampal formation of adult male mice Brain Behav. Immun. 28 2013 196 206
6. B.S. McEwen, and P.J. Gianaros Stress- and allostasis-induced brain plasticity Annu. Rev. Med. 62 2011 431 445
7. J.E. Grant, N. Fineberg, M. van Ameringen, D. Cath, H. Visser, L. Carmi, S. Pallanti, E. Hollander, and A.J. van Balkom New treatment models for compulsive disorders Eur. Neuropsychopharmacol. 15 2015 358 362
8. J.I. Koenig, B. Kirkpatrick, and P. Lee Glucocorticoid hormones and early brain developmentin schizophrenia Neuropsychopharmacology 27 2002 309 318
9. O. Kofman The role of prenatal stress in the etiology of developmental behavioural disorders Neurosci. Biobehav. Rev. 26 2002 457 470
10. M. Weinstock Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis? Neurosci. Biobehav. Rev. 21 1997 1 10
11. M. Weinstock Alterations induced by gestational stress in brain morphology and behaviour of the offspring Prog. Neurobiol. 65 2001 427 451
12. M. Weinstock The long-term behavioural consequences of prenatal stress Neurosci. Biobehav. Rev. 32 2008 1073 1086
13. S. Maccari, M. Darnaudery, S. Morley-Fletcher, A.R. Zuena, C. Cinque, and O. Van Reeth Prenatal stress and longterm consequences: implications of glucocorticoid hormones Neurosci. Biobehav. Rev. 27 2003 119 127
14. M. Darnaudéry, and S. Maccari Epigenetic programming of the stress response in male and female rats by prenatal restraint stress Brain Res. Rev. 2 2008 571 585
15. P.D. Gluckman, M.A. Hanson, C. Cooper, and K.L. Thornburg Effect of in utero and early-life conditions on adult health and disease N. Engl. J. Med. 3 2008 61 73
16. T.Y. Zhang, and M.J. Meaney Epigenetics and the environmental regulation of the genome and its function Annu. Rev. Psychol. 61 2010 439 466
17. A.C. Foster, R. Gill, J.A. Kemp, and G.N. Woodruff Systemic administration of MK-801 prevents N-methyl-d-aspartate-induced neuronal degeneration in rat brain Neurosci. Lett. 76 1987 307 311
18. S.J. Lupien, B.S. McEwen, M.R. Gunnar, and C. Heim Effects of stress throughout the lifespan on the brain, behaviour and cognition Nat. Rev. Neurosci. 10 2009 434 445
19. R.C. Kessler, S. Avenevoli, and K. RiesMerikangas Mood disorders in children and adolescents: an epidemiologic perspective Biol. Psychiatry 49 2001 1002 1014
20. M. King, and P. Bearman Diagnostic change and the increased prevalence of autism Int. J. Epidemiol. 38 2009 1224 1234
21. R.M. Sapolsky, L.M. Romero, and A.U. Munck How do glucocorticoids influence stress responses? Integrating permissive suppressive, stimulatory and preparative actions Endocr. Rev. 21 2000 55 89
22. E. Charmandari, C. Tsigos, and G. Chrousos Endocrinology of the stress response Annu. Rev. Physiol. 67 2005 259 284
23. C.M. Bamberger, H.M. Schulte, and G.P. Chrousos Molecular determinants of glucocorticoid receptor function and tissue sensitivity to glucocorticoids Endocr. Rev. 17 1996 245 261
24. S.M. Smith, and W.W. Vale The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress Dialogues Clin. Neurosci. 8 2006 383 395
25. P.E. Sawchenko Evidence for a local site of action for glucocorticoids in inhibiting CRF and vasopressin expression in the paraventricular nucleus Brain Res. 437 1987 253 263
26. L. Jacobson, and R. Sapolsky The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis Endocr. Rev. 12 1991 118 134
27. S. Deppermann, H. Storchak, A.J. Fallgatter, and A.-C. EhliS Stress-induced neuroplasticity: (mal)adaptation to adverse life events in patients with PTSD - a critical overview Neuroscience 283 2014 166 177
28. A. Ratka, W. Sutanto, M. Bloemers, and E.R. de Kloet On the role of brain mineralocorticoid (type I) and glucocorticoid (type II) receptors in neuroendocrine regulation Neuroendocrinology 50 1989 117 123
29. L. Arborelius, M.J. Owens, P.M. Plotsky, and C.B. Nemeroff The role of corticotropin-releasing factor in depression and anxiety disorders J. Endocrinol. 160 1999 1 12
30. M.N. de Lima, J. Presti-Torres, G. Vedana, L.A. Alcalde, L. Stertz, G.R. Fries, R. Roesler, M.L. Andersen, J. Quevedo, F. Kapczinski, and N. Schröder Early life stress decreases hippocampal BDNF content and exacerbates recognition memory deficits induced by repeated D-amphetamine exposure Behav. Brain Res. 224 2011 100 106
31. P. Smirnaki, M.A. Magiakou, Pregnancy- maternal and perinatal stress- effects of. (2007) Encyclopedia of Stress, George Fink, 2 da ed., vol. 3: 165-73.
32. B.E. Lee, M. Ha, H. Park, Y.C. Hong, Y. Kim, Y.J. Kim, and E.H. Ha Psychosocial work stress during pregnancy and birth weight Paediatr. Perinat. Epidemiol. 25 2011 246 254
33. S. Maccari, M. Vallée, V. Mayo, and M. Le Moal Prenatal stress during pregnancy and metabolic consequences in adult rats Arch. Pediatr. 4 2 Suppl. (2) 1997 138s 140s
34. M. Vallée, W. Mayo, F. Dellu, M. Le Moal, H. Simon, and S. Maccari Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion J. Neurosci. 17 1997 2626 2636
35. A.R. Zuena, J. Mairesse, P. Casolini, C. Cinque, G.S. Alemà, S. Morley-Fletcher, V. Chiodi, L.G. Spagnoli, R. Gradini, A. Catalani, F. Nicoletti, and S. Maccari Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats PLoS One 3 2008 e2170
36. R. Ruiz, and C. Avant Effects of maternal prenatal stress on infant outcomes ANS Adv. Nurs. Sci. 28 2005 345 355
37. B.R. Mueller, and T.L. Bale Impact of prenatal stress on long term body weight is dependent on timing and maternal sensitivity Physiol. Behav. 88 2006 605 614
38. D.L. Van den Hove, H. Steinbusch, A. Scheepens, B.W. Vande, L. Kooiman, B. Boosten, J. Prickaerts, and C. Blanco Prenatal stress and neonatal rat brain development Dev. Neurosci. 27 2005 313 320
39. J. Wu, T.B. Song, Y.J. Li, H.S. He, L. Ge, and L.R. Wang Prenatal restraint stress impairs learning and memory and hippocampal PKCbeta1 expression and translocation in offspring rats Brain Res. 13 2007 205 213
40. D.G. Maur, C.B. Romero, B. Burdet, M.L. Palumbo, and M.A. Zorrilla-Zubilete Prenatal stress induces alterations in cerebellar nitric oxide that are correlated with deficits in spatial memory in rat's offspring Neurochem. Int. 61 2012 1294 1301
41. V. Patin, B. Lordi, A. Vincent, and J. Caston Effects of prenatal stress on anxiety and social inter-actions in adult rats Brain Res. Dev. Brain Res. 160 2005 265 274
42. S. Maccari, H.J. Krugers, S. Morley-Fletcher, M. Szyf, and P.J. Brunton The consequences of early-life adversity: neurobiological: behavioural and epigenetic adaptations J. Neuroendocrinol. 26 2014 707 723
43. M. Solinas, N. Thiriet, R. El Rawas, V. Lardeux, and M. Jaber Environmental enrichment during early stages of life reduces the behavioral, neurochemical, and molecular effects of cocaine Neuropsychopharmacology 34 2009 1102 1111
44. M.J. Eckert, and W.C. Abraham Effects of environmental enrichment exposure on synaptic transmission and plasticity in the hippocampus Curr. Top. Behav. Neurosci. 15 2013 165 187
45. T.R. Guilarte, C.D. Toscano, J.L. Mcglothan, and S.A. Weaver Environmental enrichment reverses cognitive and molecular deficits induced by developmental lead exposure Ann. Neurol. 53 2003 50 56
46. P. Chapillon, V. Patin, V. Roy, A. Vincent, and J. Caston Effects of pre- and postnatal stimulation on developmental, emotional, and cognitive aspects in rodents: a review Dev. Psychobiol. 41 2002 373 387
47. V. Lemaire, S. Lamarque, M. Le Moal, P.V. Piazza, and D.N. Abrous Postnatal stimulation of the pups counteracts prenatal stressinduced deficits in hippocampal neurogenesis Biol. Psychiatry 59 2006 786 792
48. K.J. O'Donnell, V. Glover, J.D. Holbrook, and T.G. O'Connor Maternal prenatal anxiety and child brain-derived neurotrophic factor (BDNF) genotype: effects on internalizing symptoms from 4 to 15 years of age Dev. Psychopathol. 26 2014 1255 1266
49. J. Lehmann, C.R. Pryce, A.L. Jongen-Relo, T. Stohr, H.H. Pothuizen, and J. Feldon Comparison of maternal separation and early handlingin terms of their neurobehavioral effects in aged rats Neurobiol. Aging 23 2002 457 466
50. S. Levine, J.A. Chevalier, and S.J. Korchin The effects of early shock andhandling on later avoidance learning J. Pers. 24 1956 475 493
51. F.S. Hall Social deprivation of neonatal adolescent, and adult rats hasdistinct neurochemical and behavioral consequences Crit. Rev. Neurobiol. 12 1998 129 162
52. E. Roman, L. Gustafsson, M. Berg, and I. Nylander Behavioral profiles and stress-induced corticosteroid secretion in male Wistar rats subjected to short and prolonged periods of maternal separation Horm. Behav. 50 2006 736 747
53. A. Anisman, and K. Matheson Stress, depression, and anhedonia: caveats concerning animal models Neurosci. Biobehav. Rev. 29 2005 525 546
54. C. Heim, G. Meinlschmidt, and C.B. Nemeroff Neurobiology of early-life stress Psych. Ann. 33 2003 1 10
55. R. Gilbert, A. Kemp, J. Thoburn, P. Sidebotham, L. Radford, D. Glaser, and H.L. Macmillan Recognising and responding to child maltreatment Lancet 373 2009 167 180
56. E. McCrory, S.A. De Brito, and E. Viding The impact of childhood maltreatment: a review of neurobiological and genetic factors Front. Psychiatry 2 2011 48
57. R.F. Anda, V.J. Felitti, J.D. Bremner, J.D. Walker, C. Whitfield, B.D. Perry, S.R. Dube, and W.H. Giles The enduring effects of abuse and related adverse experiences in childhood Eur. Arch. Psychiat. Clin. Neurosci. 256 2006 174 186
58. V.J. Felitti, R.F. Anda, D. Nordenberg, D.F. Williamson, A.M. Spitz, V. Edwards, M.P. Koss, and J.S. Marks Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The adverse childhood experiences (ACE) study Am. J. Prev. Med. 14 1998 245 258
59. C. Heim, and C.B. Nemeroff The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies Biol. Psychiatry 49 2001 1023 1039
60. C. Heim, T. Mletzko, D. Purselle, D.L. Musselman, and C.B. Nemeroff The dexamethasone/corticotropinreleasing factor test in men with major depression: role of childhood trauma Biol. Psychiatry 63 2008 398 405
61. C. Heim, P.M. Plotsky, and C.B. Nemeroff Importance of studying the contributions of early adverse experience to neurobiological findings in depression Neuropsychopharmacology 29 2004 641 648
62. J.W. Jahng An animal model of eating disorders associated with stressful experience in early life Horm. Behav. 59 2011 213 220
63. D.A. Gutman, and C.B. Nemeroff Neurobiology of early life stress: rodent studies Semin. Clin. Neuropsychiatry 7 2002 89 95
64. R. Benediktsson, A.A. Calder, C.R. Edwards, and J.R. Seckl Placental 11 beta-hy-droxysteroid dehydrogenase: a key regulator of fetal glucocorticoid exposure Clin. Endocrinol. (Oxf.) 46 1997 161 166
65. L.A. Welberg, L.V. Thrivikraman, and P.M. Plotsky Chronic maternal stress inhibits the capacity to up-regulate placental 11 beta-hydroxysteroid dehydrogenase type 2 activity J. Endocrinol. 186 2005 R7 R12
66. J. Mairesse, J. Lesage, C. Breton, B. Breant, T. Hahn, M. Darnaudery, S.L. Dickson, J. Seckl, B. Blondeau, D. Vieau, S. Maccari, and O. Viltart Maternal stress alters endocrine function of the feto-placental unit in rats Am. J. Physiol. Endocrinol. Metab. 292 2007 E1526 E1533
67. P.J. Brunton, J.A. Russell, and A.J. Douglas Adaptive responses of the maternal hypothalamic-pituitary-adrenal axis during pregnancy and lactation J. Neuroendocrinol. 20 2008 764 776
68. A. Barbazanges, P.V. Piazza, M. Le Moal, and S. Maccari Maternal glucocorticoid secretion mediates long-term effects of prenatal stress J. Neurosci. 16 1996 3943 3949
69. L.A. Welberg, J.R. Seckl, and M.C. Holmes Inhibition of 11beta-hydroxysteroid dehydrogenase, the foeto-placental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxiety-like behaviour in the offspring Eur. J. Neurosci. 12 2000 1047 1054
70. F. Fumagalli, R. Molteni, G. Racagni, and M.A. Riva Stress during development: impact on neuroplasticity and relevance to psychopathology Prog. Neurobiol. 81 2007 197 217
71. C.A. Sandman, P.D. Wadhwa, A. Chicz-Demet, C. Dunkel-Schetter, and M. Porto Maternal stress, HPA activity, and fetal/infant outcome Ann. N. Y. Acad. Sci. 814 1997 266 275
72. B.G. Robinson, R.L. Emanuel, D.M. Frim, and J.A. Majzoub Glucocorticoid stimulates expression of corticotropin-releasing hormone gene in human placenta Proc. Natl. Acad. Sci. U. S. A. 85 1988 5244 5248
73. T. Fujioka, Y. Sakata, K. Yamaguchi, T. Shibasaki, H. Kato, and S. Nakamura The effects of prenatal stress on the development of hypothalamic paraventricular neurons in fetal rats Neuroscience 92 1999 1079 1088
74. R.L. Huot, M.E. Gonzalez, C.O. Ladd, K.V. Thrivikraman, and P.M. Plotsky Foster litters prevent hypothalamic-pituitary-adrenal axis sensitization mediated by neonatal maternal separation Psychoneuroendocrinology 29 2004 279 289
75. E. Kitraki, O. Kremmyda, D. Youlatos, M.N. Alexis, and C. Kittas Gender-dependent alterations in corticosteroid receptor status and spatial performance following 21 days of restraint stress Neuroscience 125 2004 47 55
76. W. Sutanto, P. Rosenfeld, E.R. de Kloet, and S. Levine Long term effects of neonatal maternal deprivation and ACTH on hippocampal mineralocorticoid and glucocorticoid receptors Brain Res. Dev. Brain Res. 92 1996 156 163
77. R.M. Vázquez, H. Van Oers, S. Levine, and H. Akil Regulation of glucocorticoid and mineralocorticoid receptor mRNAs in the hippocampus of the maternally deprived infant rat Brain Res. 731 1996 79 90
78. M.J. Meaney, S. Bhatnagar, J. Diorio, S. Larocque, D. Francis, D. O'Donnell, N. Shanks, S. Sharma, J. Smythe, and V. Viau Molecular basis for the development of individual differences in the hypothalamic-pituitary-adrenal stress response Cell Mol. Neurobiol. 1993
79. A. Kapoor, and S.G. Matthews Prenatal stress modifies behavior and hypothalamic-pituitary-adrenal function in female guinea pig offspring: effects of timing of prenatal stress and stage of reproductive cycle Endocrinology 149 2008 6406 6415
80. S. Maccari, P.V. Piazza, M. Kabbaj, A. Barbazanges, H. Simon, and M. Le Moal Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress J. Neurosci. 15 1995 110 116
81. A.J. Grippo, T.G. Beltz, R.M. Weiss, and A.K. Johnson The effects of chronic fluoxetine treatment on chronic mild stress induced cardiovascular changes and anhedonia Biol. Psychiatry 59 2006 309 316
82. T. Nishioka, J.A. Anselmo-Franci, P. Li, M.F. Callahan, and M. Morris Stress increases oxytocin release within thehypothalamicparaventricular nucleus Brain Res. 781 1998 56 60
83. S.E. Taylor, G.C. Gonzaga, L.C. Klein, P. Hu, G.A. Greendale, and T.E. Seeman Relation of oxytocin to psychological stress responses and hypothalamic-pituitary-adrenocortical axis activity in older women Psychosom. Med. 68 2006 238 245
84. R.J. Windle, Y.M. Kershaw, N. Shanks, S.A. Wood, S.L. Lightman, and C.D. Ingram Oxytocin attenuates stress-induced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo-pituitary-adrenal activity J. Neurosci. 24 2004 2974 2982
85. R.J. Windle, L.E. Gamble, Y.M. Kershaw, S.A. Wood, S.L. Lightman, and C.D. Ingram Gonadal steroid modulation of stress-induced hypothalamo-pituitary-adrenal activity and anxiety behavior: role of central oxytocin Endocrinology 147 2006 2423 2431
86. D.A. Slattery, and I.D. Neumann Chronic icv oxytocin attenuates the pathological high anxiety state of selectively bred Wistar rats Neuropharmacology 58 2010 56 61
87. M. Lukas, I. Toth, S.O. Reber, D.A. Slattery, A.H. Veenema, and I.D. Neumann The neuropeptide oxytocin facilitates pro-social behavior and prevents social avoidance in rats and mice Neuropsychopharmacology 36 2011 2159 2168
88. M. Heinrichs, T. Baumgartner, C. Kirschbaum, and U. Ehlert Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress Biol. Psychiatry 54 2003 1389 1398
89. B. Ditzen, M. Schaer, B. Gabriel, G. Bodenmann, U. Ehlert, and M. Heinrichs Intranasal oxytocin increases positive communication and reduces cortisol levels during couple conflict Biol. Psychiatry 65 2009 728 731
90. M. Quirin, J. Kuhl, and R. Dusing Oxytocin buffers cortisol responses to stress in individuals with impaired emotion regulation abilities Psychoneuroendocrinology 36 2011 898 904
91. A.M. Linnen, M.A. Ellenbogen, C. Cardoso, and R. Joober R, Intranasal oxytocin and salivary cortisol concentrations during social rejection in university students Stress 15 2012 393 402
92. I. Liberzon, and E.A. Young Effects of stress and glucocorticoids on CNS oxytocin receptor binding Psychoneuroendocrinology 22 1997 411 422
93. S. Korsching The neurotrophic factor concept: a reexamination J. Neurosci. 13 1993 2739 2748
94. S. Mayeur, M.A. Lukaszewski, C. Breton, L. Storme, C. Junien, D. Vieau, and J. Lesage BDNF in feto-placental development Med. Sci. (Paris) 27 2011 251 252
95. K. Kawamura, N. Kawamura, W. Sato, J. Fukuda, J. Kumagai, and T. Tanaka Brain-derivedneurotrophic factor promotes implantation and subsequent placental development by stimulating trophoblast cell growth and survival Endocrinology 150 2009 3774 3782
96. K. Kawamura, N. Kawamura, Y. Kumazawa, J. Kumagai, T. Fujimoto, and T. Tanaka Brain-derived neurotrophic factor/tyrosine kinase B signaling regulates human trophoblast growth in an in vivo animal model of ectopic pregnancy Endocrinology 152 2011 1090 1100
97. I. Kodomari, E. Wada, S. Nakamura, and K. Wada Maternal supply of BDNF to mouse fetal brain through the placenta Neurochem. Int. 54 2009 95 98
98. K. Hashimoto, H. Koizumi, M. Nakazato, E. Shimizu, and M. Iyo Role of brain-derived neurotrophic factor in eating disorders: recent findings and its pathophysiological implications Prog. Neuropsychopharmacol. Biol. Psychiatry 29 2005 499 504
99. T. Numakawa, E. Kumamaru, N. Adachi, Y. Yagasaki, A. Izumi, and H. Kunugi Glucocorticoid receptor interaction with TrkB promotes BDNF-triggered PLC-gamma signaling for glutamate release via a glutamate transporter Proc. Natl. Acad. Sci. U. S. A. 106 2010 647 652
100. C.T. Correia, A.M. Coutinho, A.F. Sequeira, I.G. Sousa, L.L.O. Venda, J.P. Almeida, R.L. Abreu, C. Lobo, T.S. Miguel, J. Conroy, L. Cochrane, L. Gallagher, M. Gill, S. Ennis, G.G. Oliveira, and A.M. Vicente Increased BDNF levels and NTRK2 gene association suggest a disruption of BDNF/TrkB signaling in autism Genes Brain Behav. 9 2010 841 848
101. P.F. Buckley, S. Mahadik, A. Pillai, and A. JrTerry Neurotrophins and schizophrenia Schizophr. Res. 94 2007 1 11
102. F. Angelucci, S. Brene, and A.A. Mathe BDNF in schizophrenia, depression and corresponding animal models Mol. Psychiatry 10 2005 345 352
103. B.L. Hempstead Dissecting the diverse actions of pro- and mature neurotrophins Curr. Alzheimer Res. 3 2006 19 24
104. L.F. Reichardt Neurotrophin-regulated signalling pathways Philos. Trans. R. Soc. Lond. B Biol. Sci. 361 2006 1545 1546
105. D.K. Binder, and H.E. Scharfman Brain-derived neurotrophic factor Growth Factors 22 2004 123 131
106. M. Bibel, and Y.A. Barde Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system Genes Dev. 14 2000 2919 2937
107. S. Pezet, and S.B. McMahon Neurotrophins: mediators and modulators of pain Annu. Rev. Neurosci. 29 2006 507 538
108. C. Pittenger, and R.S. Duman Stress, depression, and neuroplasticity: a convergence of mechanisms Neuropsychopharmacology 33 2008 88 109
109. A.F. Schinder, and M. Poo The neurotrophin hypothesis for synaptic plasticity Trends Neurosci. 23 2000 639 645
110. H.D. Schmidt, R.C. Shelton, and R.S. Duman Functional biomarkers of depression: diagnosis, treatment, and pathophysiology Neuropsychopharmacology 36 2011 2375 2394
111. J.D. Bremner, M. Vythilingam, E. Vermetten, S.M. Southwick, T. McGlashan, A. Nazeer, S. Khan, L.V. Vaccarino, R. Soufer, P.K. Garg, C.K. Ng, L.H. Staib, J.S. Duncan, and D.S. Charney MRI and PET study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder Am. J. Psychiatry 160 2003 924 932
112. R. Grassi-Oliveira, L.M. Stein, R.P. Lopes, A.L. Teixeira, and M.E. Bauer Low plasma brain-derived neurotrophic factor and childhood physical neglect are associated with verbal memory impairment in major depression-a preliminary report Biol. Psychiatry 64 2008 281 285
113. Q. Wang, F. Shao, and W. Wang Maternal separation produces alterations of forebrain brain-derived neurotrophic factor expression in differently aged rats Front. Mol. Neurosci. 8 2015 49
114. D. Liu, J. Diorio, J.C. Day, D.D. Francis, and M.J. Meaney Maternal care, hippocampal synaptogenesis and cognitive development in rats Nat. Neurosci. 3 2000 799 806
115. Z.Y. Chen, D. Jing, K.G. Bath, A. Ieraci, T. Khan, C.J. Siao, D.G. Herrera, M. Toth, C. Yang, B.S. McEwen, B.L. Hempstead, and F.S. Lee Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior Science 314 2006 140 143
116. S. Murakami, H. Imbe, Y. Morikawa, C. Kubo, and E. Senba Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly Neurosci. Res. 53 2005 129 139
117. M.F. Egan, M. Kojima, J.H. Callicott, T.E. Goldberg, B.S. Kolachana, A. Bertolino, E. Zaitsev, B. Gold, D. Goldman, M. Dean, B. Lu, and D.R. Weinberger The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function Cell 112 2003 257 269
118. V.G. Barros, M.A. Berger, I.D. Martijena, M.I. Sarchi, A.A. Perez, V.A. Molina, F.I. Tarazi, and M.C. Antonelli Early adoption modifies the effects of prenatal stress on dopamine and glutamate receptors in adult rat brain J. Neurosci. Res. 76 2004 488 496
119. C.H. Vinkers, R.S. Oosting, M.J. van Bogaert, B. Olivier, and L. Groenink Early-life blockade of 5-HT(1A) receptors alters adult anxiety behavior and benzodiazepine sensitivity Biol. Psychiatry 67 2010 309 316
120. M. Popoli, Z. Yan, B.S. McEwen, and G. Sanacora The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission Nat. Rev. Neurosci. 13 2013 22 37
121. C.J. Huppertz-Kessler, J. Poeschl, R. Hertel, K. Unsicker, and J. Schenkel Effects of a new postnatal stress model on monoaminergic neurotransmitters in rat brains Brain Dev. 34 2012 274 279
122. V. Lemaire, M. Koehl, M. Le Moal, and D.N. Abrous Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus Proc. Natl. Acad. Sci. U. S. A. 97 2000 11032 11037
123. G.H. Son, D. Geum, S. Chung, E.J. Kim, J.H. Jo, C.M. Kim, K.H. Lee, H. Kim, S. Choi, H.T. Kim, C.J. Lee, and K. Kim Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity J. Neurosci. 26 2006 3309 3318
124. E. Fride, Y. Dan, M. Gavish, and M. Weinstock Prenatal stress impairs maternal behavior in a conflict situation and reduces hippocampal benzodiazepine receptors Life Sci. 36 1985 2103 2109
125. D.L. Van den Hove, H.W. Steinbusch, A. Scheepens, W.D. Van de Berg, L.A. Kooiman, B.J. Boosten, J. Prickaerts, and C.E. Blanco Prenatal stress and neonatal rat brain development Neuroscience 137 2006 145 155
126. L.P. Chandravanshi, R.S. Yadav, R.K. Shukla, A. Singh, A. Sultana, A.B. Pant, D. Parmar, and V.K. Khanna Reversibility of changes in brain cholinergic receptors and acetylcholinesterase activity in rats following early life arsenic exposure Int. J. Dev. Neurosci. 34 2014 60 75
127. P. Huttunen Microdialysis of extracellular noradrenaline in the hippocampus of the rat after long-term alcohol intake Brain Res. 560 1991 225 228
128. R.E. Bowman, N.J. MacLusky, Y. Sarmiento, M. Frankfurt, M. Gordon, and V.N. Luine Sexually dimorphic effects of prenatal stress on cognition, hormonal responses, and central neurotransmitters Endocrinology 145 2004 3778 3787
129. Y. Wang, Y. Ma, J. Hu, W. Cheng, H. Jiang, X. Zhang, M. Li, J. Ren, and X. Li Prenatal chronic mild stress induces depression-like behavior and sex-specific changes in regional glutamate receptor expression patterns in adult rats Neuroscience 301 2015 363 374
130. E. Adrover, M.E. Pallarés, C.J. Baier, M.C. Monteleone, F.A. Giuliani, H.S. Waagepetersen, M.A. Brocco, R. Cabrera, U. Sonnewald, A. Schousboe, and M.C. Antonelli Glutamate neurotransmission is affected in prenatally stressed offspring Neurochem. Int. 88 2015 73 87
131. M.M. Odeon, M. Andreu, L. Yamauchi, M. Grosman, and G.B. Acosta Chronic postnatal stress induces voluntary alcohol intake and modifies glutamate transporters in adolescent rats Stresss 18 2015 427 434
132. T. Uchida, T. Furukawa, S. Iwata, Y. Yanagawa, and A. Fukuda Selective loss of parvalbumin-positiveGABAergic interneurons in the cerebral cortex of maternally stressed Gad1-heterozygousmouse offspring Transl. Psychiatry 4 2014 e371
133. S. Giovanoli, L. Weber, and U. Meyer Single and combined effects of prenatal immune activationand peripubertal stress on parvalbumin and reelin expression in the hippocampal formation Brain Behav. Immun. 40 2014 48 54
134. M.M. Odeon, A.E. Salatino, and G.B. Acosta Consequences of early adverse life events on GABAergic neurons produce long term changes in brain function Trends Comp. Biochem. Physiol. 15 2011 67 72
135. J.P. Kiss, and E.S. Vizi Nitric oxide: a novel link between synaptic and nonsynaptic transmission Trends Neurosci. 24 2001 211 215
136. R.D. Hawkins, H. Son, and O. Arancio Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus Prog. Brain Res. 118 1998 155 172
137. 2+ in the induction of cerebellar long-term depression Neuron 18 1997 1025 1038
138. A.L. Tomat, L.C. Veiras, S. Aguirre, H. Fasoli, R. Elesgaray, C. Caniffi, M.A. Costa, and C.T. Arranz Mild zinc deficiency in male and female rats: early postnatal alterations in renal nitric oxide system and morphology Nutrition 29 2013 568 573
139. Z. Feng, X. Zou, H. Jia, X. Li, Z. Zhu, X. Liu, P. Bucheli, O. Ballevre, Y. Hou, W. Zhang, J. Wang, Y. Chen, and J. Liu Maternal docosahexaenoic acid feeding protects against impairment of learning and memory and oxidative stress in prenatally stressed rats: possible role of neuronal mitochondria metabolism Antioxid. Redox Signal. 16 2012 275 289
140. F.S. Bersani, O.M. Wolkowitz, D. Lindqvist, R. Yehuda, J. Flory, L.M. Bierer, I. Makotine, D. Abu-Amara, M. Coy, V.I. Reus, E.S. Epel, C. Marmar, and S.H. Mellon Global arginine bioavailability a marker of nitric oxide synthetic capacity, is decreased in PTSD and correlated with symptom severity and markers of inflammation Brain Behav. Immun. 1591 2015 30041 30046
141. A. Bird Perceptions of epigenetics Nature 447 2007 396 398
142. J. Bohacek, and I.M. Mansuy Epigenetic inheritance of disease and disease risk Neuropsychopharmacology 38 2013 220 236
143. J.M. Levenson, K.J. O'Riordan, K.D. Brown, M.A. Trinh, D.L. Molfese, and J.D. Sweatt Regulation of histone acetylation during memory formation in the hippocampus J. Biol. Chem. 279 2004 40545 40559
144. I. Branchi, N. Francia, and E. Alleva Epigenetic control of neurobehavioural plasticity: the role of neurotrophins Behav. Pharmacol. 15 2004 353 362
145. K.E. Dennis, and P. Levitt Regional expression of brain derived neurotrophic factor (BDNF) is correlated with dynamic patterns of promoter methylation in the developing mouse forebrain Brain Res. Mol. Brain Res. 140 2005 1 9
146. T.L. Roth, F.D. Lubin, A.J. Funk, and J.D. Sweatt Lasting epigenetic influence of early-life adversity on the BDNF gene Biol. Psychiatry 65 2009 760 769
147. S. St Cyr, and P.O. MacGowan Programming of stress-related behavior and epigenetic neural gene regulation in mice offspring through maternal exposure to predator odor Front. Behav. Neurosci. 9 2015 145
148. R.H. van der Doelen, I.A. Arnoldussen, H. Ghareh, L. van Och, J.R. Homberg, and T. Kozicz Early life adversity and serotonin transporter gene variation interact to affect DNA methylation of the corticotropin-releasing factor gene promoter region in the adult rat brain Dev. Psychopathol. 27 2015 123 135
149. J.E. Oh, N. Chambwe, S. Klein, J. Gal, S. Andrews, G. Gleason, R. Shaknovich, A. Melnick, F. Campagne, and M. Toth Differential gene body methylation and reduced expression of cell adhesion and neurotransmitter receptor genes in adverse maternal environment Transl. Psychiatry 2013 3
150. X.H. Zhang, N. Jia, X.Y. Zhao, G.K. Tang, L.X. Guan, D. Wang, H.L. Sun, H. Li, and Z.L. Zhu Involvement of pGluR1, EAAT2 and EAAT3 in offspring depression induced by prenatal stress Neuroscience 250 2013 333 341
151. M.C. Monteleone, E. Adrover, M.E. Pallarés, M.C. Antonelli, A.C. Frasch, and M.A. Brocco Prenatal stress changes the glycoprotein GPM6A gene expression and induces epigenetic changes in rat offspring brain Epigenetics 19 2013 152 160
152. L. Belnoue, N. Grosjean, E. Ladevèze, D.N. Abrous, and M. Koehl Prenatal stress inhibits hippocampal neurogenesis but spares olfactory bulb neurogenesis PLoS One 8 2013 e72972
153. P.O. McGowan, A. Sasaki, A.C. D'Alessio, S. Dymov, B. Labonté, M. Szyf, G. Turecki, and M.J. Meaney Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse Nat.Neurosci. 12 2009 342 348
154. C. Murgatroyd, A.V. Patchev, Y. Wu, V. Micale, Y. Bockmuhl, D. Fischer, F. Holsboer, C.T. Wotjak, O.F. Almeida, and D. Spengler Dynamic DNA methylation programs persistent adverse effects of early-life stress Nat. Neurosci. 12 2009 1559 1566
155. A.R. Tyrka, J.K. Lee, J.A. Graber, A.M. Clement, M.M. Kelly, L. DeRose, M.P. Warren, and J. Brooks-Gunn Neuroendocrine predictors of emotional and behavioral adjustment in boys: longitudinal follow-up of a community sample Psychoneuroendocrinology 37 2012 2042 2046
156. S.R. Alt, J.D. Turner, M.D. Klok, O.C. Meijer, E.A. Lakke, R.H. Derijk, and C.P. Muller Differential expression of glucocorticoid receptor transcripts in major depressive disorder is not epigenetically programmed Psychoneuroendocrinology 35 2010 544 556
157. B. Labonte, M. Suderman, G. Maussion, L. Navaro, V. Yerko, I. Mahar, A. Bureau, N. Mechawar, M. Szyf, M.J. Meaney, and G. Turecki Genome-wide epigenetic regulation by early-life trauma Arch. Gen. Psychiatry 69 2012 722 731
158. W.S. Xu, R.B. Parmigiani, and P.A. Marks Histone deacetylase inhibitors: molecular mechanisms of action Oncogene 26 2007 5541 5552
159. A.G. Kazantsev, and L.M. Thompson Therapeutic application of histone deacetylase inhibitors for central nervous system disorders Nat. Rev. Drug Discov. 7 2008 854 868
160. M. Dokmanovic, C. Clarke, and P.A. Marks Histone deacetylase inhibitors: overview and perspectives Mol. Cancer Res. 5 2007 981 989
161. M. Dragunow, J.M. Greenwood, R.E. Cameron, P.J. Narayan, S.J. O'Carroll, A.G. Pearson, and H.M. Gibbons Valproic acid induces caspase 3-mediated apoptosis in microglial cells Neuroscience 140 2006 1149 1156
162. P.S. Chen, C.C. Wang, C.D. Bortner, G.S. Peng, X. Wu, H. Pang, R.B. Lu, P.W. Gean, D.M. Chuang, and J.S. Hong Valproic acid and other histone deacetylase inhibitors induce microglial apoptosis and attenuate lipopolysaccharide-induced dopaminergic neurotoxicity Neuroscience 149 2007 203 212
163. H.J. Kim, M. Rowe, M. Ren, J.S. Hong, P.S. Chen, and D.M. Chuang Histone deacetylase inhibitors exhibit anti-inflammatory and neuroprotective effects in a rat permanent ischemic model of stroke: multiple mechanisms of action J. Pharmacol. Exp. Ther. 321 2007 892 901
164. P.S. Chen, G.S. Peng, G. Li, S. Yang, X. Wu, C.C. Wang, B. Wilson, R.B. Lu, P.W. Gean, D.M. Chuang, and J.S. Hong Valproate protects dopaminergic neurons in midbrain neuron/glia cultures by stimulating the release of neurotrophic factors from astrocytes Mol. Psychiatry 11 2006 1116 11125
165. X. Wu, P.S. Chen, S. Dallas, B. Wilson, M.L. Block, C.C. Wang, H. Kinyamu, N. Lu, X. Gao, Y. Leng, D.M. Chuang, W. Zhang, R.B. Lu, and J.S. Hong Histone deacetylase inhibitors up-regulate astrocyte GDNF and BDNF gene transcription and protect dopaminergic neurons Int. J. Neuropsychopharmacol. 11 2008 1123 1134
166. M. Kilgore, C.A. Miller, D.M. Fass, K.M. Hennig, S.J. Haggarty, J.D. Sweatt, and G. Rumbaugh Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer's disease Neuropsychopharmacology 35 2010 870 880
167. S.Y. Cong, B.A. Pepers, B.O. Evert, D.C. Rubinsztein, R.A. Roos, G.J. van Ommen, and J.C. Dorsman Mutant huntingtin represses CBP but not p300, by binding and protein degradation Mol. Cell Neurosci. 30 2005 12 23
168. R.N. Saha, and K. Pahan HATs and HDACs in neurodegeneration: a tale of disconcerted acetylation homeostasis Cell Death Differ. 13 2005 539 550
169. D.C. Lagace, and M.W. Nachtigal Inhibition of histone deacetylase activity by valproic acid blocks adipogenesis J. Biol. Chem. 279 2004 18851 18860
170. R.A. Blaheta, M. Michaelis, P.H. Driever, and J. Cinatl Jr. Evolving anticancer drug valproic acid: insights into the mechanism and clinical studies Med. Res. Rev. 25 2005 383 397
171. G. Koren, A.A. Nava-Ocampo, M.E. Moretti, R. Sussman, and I. Nulman Major malformations with valproic acid Can. Fam. Phys. 52 2006 444 447
172. J. Koch, S. Gärtner, C.M. Li, L.E. Quintern, K. Bernardo, O. Levran, D. Schnabel, R.J. Desnick, E.H. Schuchman, and K. Sandhoff Molecular cloning and characterization of a full-length complementary DNA encoding human acid ceramidase. Identification ofthe first molecular lesion causing Farber disease J. Biol. Chem. 271 1996 33110 33115
173. P.G. Williams, and J.H. Hersh A male with fetal valproate syndrome and autism Dev. Med. Child. Neurol. 39 1997 632 634
174. A.D. Rasalam, H. Hailey, J.H. Williams, S.J. Moore, P.D. Turnpenny, D.J. Lloyd, and J.C. Dean Characteristics of fetal anticonvulsant syndrome associated autistic disorder Dev. Med. Child. Neurol. 47 2005 551 555
175. N. Carey, and N.B. La Thangue Histone deacetylase inhibitors: gathering pace Curr. Opin. Pharmacol. 6 2006 369 375
176. M. Minamiyama, M. Katsuno, H. Adachi, M. Waza, C. Sang, Y. Kobayashi, F. Tanaka, M. Doyu, A. Inukai, and G. Sobue Sodium butyrate ameliorates phenotypic expression in a transgenic mouse model of spinal and bulbar muscular atrophy Hum. Mol. Genet. 13 2004 1183 1192
177. F.A. Schroeder, C.L. Lin, W.E. Crusio, and S. Akbarian Antidepressant-like effects of the histone deacetylase inhibitor sodium butyrate, in the mouse Biol. Psychiatry 62 2007 55 64
178. H. Gagliano, R. Delgado-Morales, A. Sanz-Garcia, and A. Armario High doses of the histone deacetylase inhibitor sodium butyrate trigger a stress-like response Neuropharmacology 79 2014 75 82
179. C. Nasca, D. Xenos, Y. Barone, A. Caruso, S. Scaccianoce, F. Matrisciano, G. Battaglia, A.A. Mathé, A. Pittaluga, L. Lionetto, M. Simmaco, and F. Nicoletti l-acetylcarnitine causes rapid antidepressant effects through the epigenetic induction of mGlu2 receptors Proc. Natl. Acad. Sci. U. S. A. 110 2013 4804 4809
180. J.E. Bolden, M.J. Peart, and R.W. Johnstone Anticancer activities of histone deacetylase inhibitors Nat. Rev. Drug Discov. 5 2006 769 784