Sex-dependent programming effects of prenatal glucocorticoid treatment on the developing serotonin system and stress-related behaviors in adulthood

Neuroscience

Volumn 320, Issue , 2016, Pages 43-56

  Hiroi, R ^a,b   Carbone, D L ^a   Zuloaga, D G ^a,d   Bimonte Nelson, H A ^b   Handa, R J ^a,c  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c Department of Environmental and Radiological Health Sciences   (United States)

^d STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

anxiety depression; Dexamethasone; dorsal raphe nucleus; Rat; tryptophan hydroxylase 2

Indexed keywords

DEXAMETHASONE; GLUCOCORTICOID; SEROTONIN; TPH2 PROTEIN, RAT; TRYPTOPHAN HYDROXYLASE;

AGING; ANIMAL; ANIMAL BEHAVIOR; ANXIETY; COMPLICATION; DEPRESSION; DISEASE MODEL; DORSAL RAPHE NUCLEUS; FEMALE; MALE; MENTAL STRESS; METABOLISM; PATHOPHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; RADIOIMMUNOASSAY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEXUAL DEVELOPMENT; SPRAGUE DAWLEY RAT;

AGING; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; DEPRESSION; DEXAMETHASONE; DISEASE MODELS, ANIMAL; DORSAL RAPHE NUCLEUS; FEMALE; GLUCOCORTICOIDS; MALE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RADIOIMMUNOASSAY; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEROTONIN; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL; TRYPTOPHAN HYDROXYLASE;

EID: 84957899909     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2016.01.055     Document Type: Article

References (133)

1. Abrams J.K., Johnson P.L., Hollis J.H., Lowry C.A. Anatomic and functional topography of the dorsal raphe nucleus. Ann N Y Acad Sci 2004, 1018:46-57.
2. Adell A., Casanovas J.M., Artigas F. Comparative study in the rat of the actions of different types of stress on the release of 5-HT in raphe nuclei and forebrain areas. Neuropharmacology 1997, 36:735-741.
3. Ahima R.S., Harlan R.E. Regulation of glucocorticoid receptor immunoreactivity in the rat hippocampus by androgenic-anabolic steroids. Brain Res 1992, 585:311-314.
4. Alonso S.J., Arevalo R., Afonso D., Rodriguez M. Effects of maternal stress during pregnancy on forced swimming test behavior of the offspring. Physiol Behav 1991, 50:511-517.
5. Arpels J.C. The female brain hypoestrogenic continuum from the premenstrual syndrome to menopause. A hypothesis and review of supporting data. J Reprod Med 1996, 41:633-639.
6. Baker S., Chebli M., Rees S., Lemarec N., Godbout R., Bielajew C. Effects of gestational stress: 1. Evaluation of maternal and juvenile offspring behavior. Brain Res 2008, 1213:98-110.
7. Bandeira F., Lent R., Herculano-Houzel S. Changing numbers of neuronal and non-neuronal cells underlie postnatal brain growth in the rat. Proc Natl Acad Sci USA 2009, 106:14108-14113.
8. Bennett-Clarke C.A., Chiaia N.L., Rhoades R.W. Thalamocortical afferents in rat transiently express high-affinity serotonin uptake sites. Brain Res 1996, 733:301-306.
9. Bertoglio L.J., Carobrez A.P. Behavioral profile of rats submitted to session 1-session 2 in the elevated plus-maze during diurnal/nocturnal phases and under different illumination conditions. Behav Brain Res 2002, 132:135-143.
10. Blanco C.E., Peltz A., Staley R., Kim F. Effects of pharmacologic androgen treatment duration on glucocorticoid receptor alpha immunoreactivity of lumbosacral motor neurons in the male rat. Neuroscience 2002, 115:941-949.
11. Blizard D.A., Lippman H.R., Chen J.J. Sex differences in open-field behavior in the rat: the inductive and activational role of gonadal hormones. Physiol Behav 1975, 14:601-608.
12. Bourke C.H., Harrell C.S., Neigh G.N. Stress-induced sex differences: adaptations mediated by the glucocorticoid receptor. Horm Behav 2012, 62:210-218.
13. Bouwknecht J.A., Spiga F., Staub D.R., Hale M.W., Shekhar A., Lowry C.A. Differential effects of exposure to low-light or high-light open-field on anxiety-related behaviors: relationship to c-Fos expression in serotonergic and non-serotonergic neurons in the dorsal raphe nucleus. Brain Res Bull 2007, 72:32-43.
14. Brett L.P., Chong G.S., Coyle S., Levine S. The pituitary-adrenal response to novel stimulation and ether stress in young adult and aged rats. Neurobiol Aging 1983, 4:133-138.
15. Brown G.W., Harris T.O. Aetiology of anxiety and depressive disorders in an inner-city population. 1. Early adversity. Psychol Med 1993, 23:143-154.
16. Brown G.W., Harris T.O., Eales M.J. Social factors and comorbidity of depressive and anxiety disorders. Br J Psychiatry 1996, 50-57.
17. Brunton P.J., Russell J.A. Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring: sex-specific effects. J Neuroendocrinol 2010, 22:258-271.
18. Burgess L.H., Handa R.J. Estrogen-induced alterations in the regulation of mineralocorticoid and glucocorticoid receptor messenger RNA expression in the female rat anterior pituitary gland and brain. Mol Cell Neurosci 1993, 4:191-198.
19. Burgin K.E., Waxham M.N., Rickling S., Westgate S.A., Mobley W.C., Kelly P.T. In situ hybridization histochemistry of Ca2+/calmodulin-dependent protein kinase in developing rat brain. J Neurosci 1990, 10:1788-1798.
20. Cannizzaro C., Plescia F., Martire M., Gagliano M., Cannizzaro G., Mantia G., Cannizzaro E. Single, intense prenatal stress decreases emotionality and enhances learning performance in the adolescent rat offspring: interaction with a brief, daily maternal separation. Behav Brain Res 2006, 169:128-136.
21. Carbone D.L., Zuloaga D.G., Hiroi R., Foradori C.D., Legare M.E., Handa R.J. Prenatal dexamethasone exposure potentiates diet-induced hepatosteatosis and decreases plasma IGF-in a sex-specific fashion. Endocrinology 2012, 153:295-306.
22. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987, 162:156-159.
23. Clark M.S., McDevitt R.A., Neumaier J.F. Quantitative mapping of tryptophan hydroxylase-2, 5-HT1A, 5-HT1B, and serotonin transporter expression across the anteroposterior axis of the rat dorsal and median raphe nuclei. J Comp Neurol 2006, 498:611-623.
24. Cleasby M.E., Kelly P.A., Walker B.R., Seckl J.R. Programming of rat muscle and fat metabolism by in utero overexposure to glucocorticoids. Endocrinology 2003, 144:999-1007.
25. Darnaudery M., Maccari S. Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev 2008, 57:571-585.
26. Day H.E., Greenwood B.N., Hammack S.E., Watkins L.R., Fleshner M., Maier S.F., Campeau S. Differential expression of 5HT-1A, alpha 1b adrenergic, CRF-R1, and CRF-R2 receptor mRNA in serotonergic, gamma-aminobutyric acidergic, and catecholaminergic cells of the rat dorsal raphe nucleus. J Comp Neurol 2004, 474:364-378.
27. Detke M.J., Rickels M., Lucki I. Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology 1995, 121:66-72.
28. Diaz-Veliz G., Urresta F., Dussaubat N., Mora S. Effects of estradiol replacement in ovariectomized rats on conditioned avoidance responses and other behaviors. Physiol Behav 1991, 50:61-65.
29. Diaz-Veliz G., Urresta F., Dussaubat N., Mora S. Progesterone effects on the acquisition of conditioned avoidance responses and other motoric behaviors in intact and ovariectomized rats. Psychoneuroendocrinology 1994, 19:387-394.
30. Drake A.J., Raubenheimer P.J., Kerrigan D., McInnes K.J., Seckl J.R., Walker B.R. Prenatal dexamethasone programs expression of genes in liver and adipose tissue and increased hepatic lipid accumulation but not obesity on a high-fat diet. Endocrinology 2010, 151:1581-1587.
31. Fride E., Weinstock M. Prenatal stress increases anxiety related behavior and alters cerebral lateralization of dopamine activity. Life Sci 1988, 42:1059-1065.
32. Frye C.A., Walf A.A. Estrogen and/or progesterone administered systemically or to the amygdala can have anxiety-fear-and pain-reducing effects in ovariectomized rats. Behav Neurosci 2004, 118:306-313.
33. Frye C.A., Wawrzycki J. Effect of prenatal stress and gonadal hormone condition on depressive behaviors of female and male rats. Horm Behav 2003, 44:319-326.
34. Frye C.A., Petralia S.M., Rhodes M.E. Estrous cycle and sex differences in performance on anxiety tasks coincide with increases in hippocampal progesterone and 3alpha,5alpha-THP. Pharmacol Biochem Behav 2000, 67:587-596.
35. Fujioka T., Fujioka A., Tan N., Chowdhury G.M., Mouri H., Sakata Y., Nakamura S. Mild prenatal stress enhances learning performance in the non-adopted rat offspring. Neuroscience 2001, 103:301-307.
36. Geula C., Mesulam M.M., Tokuno H., Kuo C.C. Developmentally transient expression of acetylcholinesterase within cortical pyramidal neurons of the rat brain. Brain Res Dev Brain Res 1993, 76:23-31.
37. Goel N., Bale T.L. Sex differences in the serotonergic influence on the hypothalamic-pituitary-adrenal stress axis. Endocrinology 2010, 151:1784-1794.
38. Greenwood B.N., Foley T.E., Day H.E., Campisi J., Hammack S.H., Campeau S., Maier S.F., Fleshner M. Freewheel running prevents learned helplessness/behavioral depression: role of dorsal raphe serotonergic neurons. J Neurosci 2003, 23:2889-2898.
39. Gutman D.A., Nemeroff C.B. Persistent central nervous system effects of an adverse early environment: clinical and preclinical studies. Physiol Behav 2003, 79:471-478.
40. Hale M.W., Bouwknecht J.A., Spiga F., Shekhar A., Lowry C.A. Exposure to high- and low-light conditions in an open-field test of anxiety increases c-Fos expression in specific subdivisions of the rat basolateral amygdaloid complex. Brain Res Bull 2006, 71:174-182.
41. Hammack S.E., Richey K.J., Schmid M.J., LoPresti M.L., Watkins L.R., Maier S.F. The role of corticotropin-releasing hormone in the dorsal raphe nucleus in mediating the behavioral consequences of uncontrollable stress. J Neurosci 2002, 22:1020-1026.
42. Handa R.J., Burgess L.H., Kerr J.E., O'Keefe J.A. Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm Behav 1994, 28:464-476.
43. Harfstrand A., Fuxe K., Cintra A., Agnati L.F., Zini I., Wikstrom A.C., Okret S., Yu Z.Y., Goldstein M., Steinbusch H., et al. Glucocorticoid receptor immunoreactivity in monoaminergic neurons of rat brain. Proc Natl Acad Sci USA 1986, 83:9779-9783.
44. Hiroi R., Neumaier J.F. Differential effects of ovarian steroids on anxiety versus fear as measured by open field test and fear-potentiated startle. Behav Brain Res 2005.
45. Hiroi R., Neumaier J.F. Differential effects of ovarian steroids on anxiety versus fear as measured by open field test and fear-potentiated startle. Behav Brain Res 2006, 166:93-100.
46. Hiroi R, Neumaier JF (2006b) Estrogen selectively decreases 5-HT1B mRNA in distinct subregions of rat dorsal raphe nucleus: Inverse association between gene expression and anxiety behavior in the open field. In: Annual Northwest Chapter Meeting of the Society for Neuroscience.
47. Hiroi R., McDevitt R.A., Neumaier J.F. Estrogen selectively increases tryptophan hydroxylase-mRNA expression in distinct subregions of rat dorsal raphe nucleus: association between gene expression and anxiety behavior in the open field. Biol Psychiatry 2006, 60:288-295.
48. Hiroi R., McDevitt R.A., Neumaier J.F. Estrogen selectively increases tryptophan hydroxylase-mRNA expression in distinct subregions of rat midbrain raphe nucleus: association between gene expression and anxiety behavior in the open field. Biol Psychiatry 2006, 60:288-295.
49. Hiroi R., McDevitt R.A., Morcos P.A., Clark M.S., Neumaier J.F. Overexpression or knockdown of rat tryptophan hyroxylase-has opposing effects on anxiety behavior in an estrogen-dependent manner. Neuroscience 2011, 176:120-131.
50. Hossain A., Hajman K., Charitidi K., Erhardt S., Zimmermann U., Knipper M., Canlon B. Prenatal dexamethasone impairs behavior and the activation of the BDNF exon IV promoter in the paraventricular nucleus in adult offspring. Endocrinology 2008, 149:6356-6365.
51. Hunter S.E., Seibenhener M.L., Wooten M.W. Atypical zeta-protein kinase c displays a unique developmental expression pattern in rat brain. Brain Res Dev Brain Res 1995, 85:239-248.
52. Ikonomidou C., Bosch F., Miksa M., Bittigau P., Vockler J., Dikranian K., Tenkova T.I., Stefovska V., Turski L., Olney J.W. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 1999, 283:70-74.
53. Imai H., Steindler D.A., Kitai S.T. The organization of divergent axonal projections from the midbrain raphe nuclei in the rat. J Comp Neurol 1986, 243:363-380.
54. Jacobs B.L., Azmitia E.C. Structure and function of the brain serotonin system. Physiol Rev 1992, 72:165-229.
55. Kazakov V.N., Kravtsov P., Krakhotkina E.D., Maisky V.A. Sources of cortical, hypothalamic and spinal serotonergic projections: topical organization within the nucleus raphe dorsalis. Neuroscience 1993, 56:157-164.
56. Kerr J.E., Beck S.G., Handa R.J. Androgens selectively modulate c-Fos messenger RNA induction in the rat hippocampus following novelty. Neuroscience 1996, 74:757-766.
57. Keshet G.I., Weinstock M. Maternal naltrexone prevents morphological and behavioral alterations induced in rats by prenatal stress. Pharmacol Biochem Behav 1995, 50:413-419.
58. Kikuchi Y., Hosono K., Yamashita J., Kawabata Y., Okubo K. Glucocorticoid receptor exhibits sexually dimorphic expression in the medaka brain. Gen Comp Endocrinol 2015, 223:47-53.
59. Kirby L.G., Lucki I. The effect of repeated exposure to forced swimming on extracellular levels of 5-hydroxytryptamine in the rat. Stress 1998, 2:251-263.
60. Kirby L.G., Allen A.R., Lucki I. Regional differences in the effects of forced swimming on extracellular levels of 5-hydroxytryptamine and 5-hydroxyindoleacetic acid. Brain Res 1995, 682:189-196.
61. Kirby L.G., Chou-Green J.M., Davis K., Lucki I. The effects of different stressors on extracellular 5-hydroxytryptamine and 5-hydroxyindoleacetic acid. Brain Res 1997, 760:218-230.
62. Kirby L.G., Rice K.C., Valentino R.J. Effects of corticotropin-releasing factor on neuronal activity in the serotonergic dorsal raphe nucleus. Neuropsychopharmacology 2000, 22:148-162.
63. Klink R., Robichaud M., Debonnel G. Gender and gonadal status modulation of dorsal raphe nucleus serotonergic neurons. Part I: effects of gender and pregnancy. Neuropharmacology 2002, 43:1119-1128.
64. Kosten T.A., Huang W., Nielsen D.A. Sex and litter effects on anxiety and DNA methylation levels of stress and neurotrophin genes in adolescent rats. Dev Psychobiol 2014, 56:392-406.
65. Laplante D.P., Barr R.G., Brunet A., Galbaud du Fort G., Meaney M.L., Saucier J.F., Zelazo P.R., King S. Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatr Res 2004, 56:400-410.
66. Lim S., Naisbitt S., Yoon J., Hwang J.I., Suh P.G., Sheng M., Kim E. Characterization of the Shank family of synaptic proteins. Multiple genes, alternative splicing, and differential expression in brain and development. J Biol Chem 1999, 274:29510-29518.
67. Lowry C.A. Functional subsets of serotonergic neurones: implications for control of the hypothalamic-pituitary-adrenal axis. J Neuroendocrinol 2002, 14:911-923.
68. Lucki I. The spectrum of behaviors influenced by serotonin. Biol Psychiatry 1998, 44:151-162.
69. Lund T.D., Rovis T., Chung W.C., Handa R.J. Novel actions of estrogen receptor-beta on anxiety-related behaviors. Endocrinology 2005, 146:797-807.
70. Maier S.F., Grahn R.E., Watkins L.R. 8-OH-DPAT microinjected in the region of the dorsal raphe nucleus blocks and reverses the enhancement of fear conditioning and interference with escape produced by exposure to inescapable shock. Behav Neurosci 1995, 109:404-412.
71. Marcondes F.K., Miguel K.J., Melo L.L., Spadari-Bratfisch R.C. Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiol Behav 2001, 74:435-440.
72. Maswood S., Barter J.E., Watkins L.R., Maier S.F. Exposure to inescapable but not escapable shock increases extracellular levels of 5-HT in the dorsal raphe nucleus of the rat. Brain Res 1998, 783:115-120.
73. McCormick C.M., Smythe J.W., Sharma S., Meaney M.J. Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Brain Res Dev Brain Res 1995, 84:55-61.
74. McGrath K.E., Seidler F.J., Slotkin T.A. Convergent control of serotonin transporter expression by glucocorticoids and cocaine in fetal and neonatal rat brain. Brain Res Dev Brain Res 1997, 104:209-213.
75. Molliver M.E. Serotonergic neuronal systems: what their anatomic organization tells us about function. J Clin Psychopharmacol 1987, 7:3S-23S.
76. Mora S., Dussaubat N., Diaz-Veliz G. Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 1996, 21:609-620.
77. Morgan M.A., Pfaff D.W. Estrogen's effects on activity, anxiety, and fear in two mouse strains. Behav Brain Res 2002, 132:85-93.
78. Morgan M.A., Schulkin J., Pfaff D.W. Estrogens and non-reproductive behaviors related to activity and fear. Neurosci Biobehav Rev 2004, 28:55-63.
79. Mueller B.R., Bale T.L. Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 2008, 28:9055-9065.
80. Muneoka K., Mikuni M., Ogawa T., Kitera K., Kamei K., Takigawa M., Takahashi K. Prenatal dexamethasone exposure alters brain monoamine metabolism and adrenocortical response in rat offspring. Am J Physiol 1997, 273:R1669-R1675.
81. Murmu M.S., Salomon S., Biala Y., Weinstock M., Braun K., Bock J. Changes of spine density and dendritic complexity in the prefrontal cortex in offspring of mothers exposed to stress during pregnancy. Eur J Neurosci 2006, 24:1477-1487.
82. Nadarajah B., Jones A.M., Evans W.H., Parnavelas J.G. Differential expression of connexins during neocortical development and neuronal circuit formation. J Neurosci 1997, 17:3096-3111.
83. Nagano M., Ozawa H., Suzuki H. Prenatal dexamethasone exposure affects anxiety-like behaviour and neuroendocrine systems in an age-dependent manner. Neurosci Res 2008, 60:364-371.
84. Nakazawa M., Koh T., Kani K., Maeda T. Transient patterns of serotonergic innervation in the rat visual cortex: normal development and effects of neonatal enucleation. Brain Res Dev Brain Res 1992, 66:77-90.
85. Nash M.W., Sugden K., Huezo-Diaz P., Williamson R., Sterne A., Purcell S., Sham P.C., Craig I.W. Association analysis of monoamine genes with measures of depression and anxiety in a selected community sample of siblings. Am J Med Genet Part B Neuropsychiatr Genet 2005, 135:33-37.
86. Nestler E.J., Barrot M., DiLeone R.J., Eisch A.J., Gold S.J., Monteggia L.M. Neurobiology of depression. Neuron 2002, 34:13-25.
87. O'Connor T.G., Heron J., Golding J., Beveridge M., Glover V. Maternal antenatal anxiety and children's behavioural/emotional problems at 4 years. Report from the Avon Longitudinal Study of Parents and Children. Br J Psychiatry 2002, 180:502-508.
88. O'Connor T.G., Heron J., Golding J., Glover V., Team A.S. Maternal antenatal anxiety and behavioural/emotional problems in children: a test of a programming hypothesis. J Child Psychol Psychiatry 2003, 44:1025-1036.
89. Okazawa H., Leyton M., Benkelfat C., Mzengeza S., Diksic M. Statistical mapping analysis of serotonin synthesis images generated in healthy volunteers using positron-emission tomography and alpha-[11C]methyl-L-tryptophan. J Psychiatry Neurosci 2000, 25:359-370.
90. Olavarria J.F., Hiroi R. Retinal influences specify cortico-cortical maps by postnatal day six in rats and mice. J Comp Neurol 2003, 459:156-172.
91. Oliveira M., Bessa J.M., Mesquita A., Tavares H., Carvalho A., Silva R., Pego J.M., Cerqueira J.J., Palha J.A., Almeida O.F., Sousa N. Induction of a hyperanxious state by antenatal dexamethasone: a case for less detrimental natural corticosteroids. Biol Psychiatry 2006, 59:844-852.
92. Palanza P. Animal models of anxiety and depression: how are females different?. Neurosci Biobehav Rev 2001, 25:219-233.
93. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic Press INC, San Diego.
94. Pigott T.A. Anxiety disorders in women. Psychiatr Clin North Am 2003, 26:621-672. vi-vii.
95. Poltyrev T., Weinstock M. Gender difference in the prevention of hyperanxiety in adult prenatally stressed rats by chronic treatment with amitriptyline. Psychopharmacology 2004, 171:270-276.
96. Prut L., Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 2003, 463:3-33.
97. Price M.L., Curtis A.L., Kirby L.G., Valentino R.J., Lucki I. Effects of corticotropin-releasing factor on brain serotonergic activity 1998, 18:492-502.
98. Ressler K.J., Nemeroff C.B. Role of serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Depression and anxiety 2000, 12(Suppl. 1):2-19.
99. Richardson H.N., Zorrilla E.P., Mandyam C.D., Rivier C.L. Exposure to repetitive versus varied stress during prenatal development generates two distinct anxiogenic and neuroendocrine profiles in adulthood. Endocrinology 2006, 147:2506-2517.
100. Robichaud M., Debonnel G. Oestrogen and testosterone modulate the firing activity of dorsal raphe nucleus serotonergic neurones in both male and female rats. J Neuroendocrinol 2005, 17:179-185.
101. Roche M, Commons KG, Peoples A, Valentino RJ Circuitry underlying regulation of the serotonergic system by swim stress. J Neurosci 2003, 23:970-977.
102. Rosa-Neto P., Diksic M., Okazawa H., Leyton M., Ghadirian N., Mzengeza S., Nakai A., Debonnel G., Blier P., Benkelfat C. Measurement of brain regional alpha-[11C]methyl-L-tryptophan trapping as a measure of serotonin synthesis in medication-free patients with major depression. Arch Gen Psychiatry 2004, 61:556-563.
103. Seckl J.R., Meaney M.J. Glucocorticoid programming. Ann N Y Acad Sci 2004, 1032:63-84.
104. Seckl J.R., Meaney M.J. Glucocorticoid "programming" and PTSD risk. Ann N Y Acad Sci 2006, 1071:351-378.
105. Sheng Z., Yanai A., Fujinaga R., Kawano J., Tanaka M., Watanabe Y., Shinoda K. Gonadal and adrenal effects on the glucocorticoid receptor in the rat hippocampus, with special reference to regulation by estrogen from an immunohistochemical view-point. Neurosci Res 2003, 46:205-218.
106. Slotkin T.A., Seidler F.J. Mimicking maternal smoking and pharmacotherapy of preterm labor: interactions of fetal nicotine and dexamethasone on serotonin and dopamine synaptic function in adolescence and adulthood. Brain Res Bull 2010, 82:124-134.
107. Slotkin T.A., Barnes G.A., McCook E.C., Seidler F.J. Programming of brainstem serotonin transporter development by prenatal glucocorticoids. Brain Res Dev Brain Res 1996, 93:155-161.
108. Slotkin T.A., Kreider M.L., Tate C.A., Seidler F.J. Critical prenatal and postnatal periods for persistent effects of dexamethasone on serotonergic and dopaminergic systems. Neuropsychopharmacology 2006, 31:904-911.
109. Steiner M., Dunn E., Born L. Hormones and mood: from menarche to menopause and beyond. J Affect Disord 2003, 74:67-83.
110. Sun H.S., Tsai H.W., Ko H.C., Chang F.M., Yeh T.L. Association of tryptophan hydroxylase gene polymorphism with depression, anxiety and comorbid depression and anxiety in a population-based sample of postpartum Taiwanese women. Genes Brain Behav 2004, 3:328-336.
111. Tobe I., Ishida Y., Tanaka M., Endoh H., Fujioka T., Nakamura S. Effects of repeated maternal stress on FOS expression in the hypothalamic paraventricular nucleus of fetal rats. Neuroscience 2005, 134:387-395.
112. Vallee M., Mayo W., Dellu F., Le Moal M., Simon H., Maccari S. Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J Neurosci 1997, 17:2626-2636.
113. Van den Bergh B.R., Marcoen A. High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. Child Dev 2004, 75:1085-1097.
114. Van den Hove D.L., Leibold N.K., Strackx E., Martinez-Claros M., Lesch K.P., Steinbusch H.W., Schruers K.R., Prickaerts J. Prenatal stress and subsequent exposure to chronic mild stress in rats; interdependent effects on emotional behavior and the serotonergic system. Eur Neuropsychopharmacol 2014, 24:595-607.
115. van der Kooy D., Hattori T. Dorsal raphe cells with collateral projections to the caudate-putamen and substantia nigra: a fluorescent retrograde double labeling study in the rat. Brain Res 1980, 186:1-7.
116. Venero J.L., Vizuete M.L., Machado A., Cano J. Developmental expression of 5-HT7 receptor mRNA in rat brain visual structures after neonatal enucleation. NeuroReport 1997, 8:1531-1535.
117. Vertes R.P. A PHA-analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol 1991, 313:643-668.
118. Villacres E.C., Wu Z., Hua W., Nielsen M.D., Watters J.J., Yan C., Beavo J., Storm D.R. Developmentally expressed Ca(2+)-sensitive adenylyl cyclase activity is disrupted in the brains of type I adenylyl cyclase mutant mice. J Biol Chem 1995, 270:14352-14357.
119. Watson J.B., Mednick S.A., Huttunen M., Wang X. Prenatal teratogens and the development of adult mental illness. Dev Psychopathol 1999, 11:457-466.
120. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., Dymov S., Szyf M., Meaney M.J. Epigenetic programming by maternal behavior. Nat Neurosci 2004, 7:847-854.
121. Weinstock M., Matlina E., Maor G.I., Rosen H., McEwen B.S. Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary adrenal system in the female rat. Brain Res 1992, 595:195-200.
122. Weinstock M. Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 2007, 32:1730-1740.
123. Weinstock M. The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev 2008, 32:1073-1086.
124. Weiser M.J., Wu T.J., Handa R.J. Estrogen receptor-beta agonist diarylpropionitrile: biological activities of R- and S-enantiomers on behavior and hormonal response to stress. Endocrinology 2009, 150:1817-1825.
125. Welberg L.A., Seckl J.R. Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol 2001, 13:113-128.
126. Welberg L.A., Seckl J.R., Holmes M.C. Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour. Neuroscience 2001, 104:71-79.
127. Yamagata M., Herman J.P., Sanes J.R. Lamina-specific expression of adhesion molecules in developing chick optic tectum. J Neurosci 1995, 15:4556-4571.
128. You J.S., Hu S.Y., Chen B., Zhang H.G. Serotonin transporter and tryptophan hydroxylase gene polymorphisms in Chinese patients with generalized anxiety disorder. Psychiatr Genet 2005, 15:7-11.
129. Zagron G., Weinstock M. Maternal adrenal hormone secretion mediates behavioural alterations induced by prenatal stress in male and female rats. Behav Brain Res 2006, 175:323-328.
130. Zavala J.K., Fernandez A.A., Gosselink K.L. Female responses to acute and repeated restraint stress differ from those in males. Physiol Behav 2011, 104:215-221.
131. Zhang X., Gainetdinov R.R., Beaulieu J.M., Sotnikova T.D., Burch L.H., Williams R.B., Schwartz D.A., Krishnan K.R., Caron M.G. Loss-of-function mutation in tryptophan hydroxylase-identified in unipolar major depression. Neuron 2005, 45:11-16.
132. Zuloaga D.G., Carbone D.L., Hiroi R., Chong D.L., Handa R.J. Dexamethasone induces apoptosis in the developing rat amygdala in an age-region-and sex-specific manner. Neuroscience 2011, 199:535-547.
133. Zuloaga D.G., Carbone D.L., Quihuis A., Hiroi R., Chong D.L., Handa R.J. Perinatal dexamethasone-induced alterations in apoptosis within the hippocampus and paraventricular nucleus of the hypothalamus are influenced by age and sex. J Neurosci Res 2012, 90:1403-1412.