Neuroendocrine control of maternal stress responses and fetal programming by stress in pregnancy

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 35, Issue 5, 2011, Pages 1178-1191

  Brunton, Paula J ^a   Russell, John A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Allopregnanolone; Anxiety type behaviour; Endogenous opioid; Hypothalamo pituitary adrenal axis; Prenatal stress

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 2; 5ALPHA PREGNANE 3,20 DIONE; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR; ENDOCANNABINOID; ESTROGEN; GLUCOCORTICOID; MESSENGER RNA; NEUROSTEROID; OPIATE; PEPTIDE; PROGESTERONE; PROLACTIN; RELAXIN; SEX HORMONE; VASOPRESSIN;

ADENOHYPOPHYSIS; AMYGDALOID NUCLEUS; ANXIETY; ARTICLE; BIOENERGY; BLOOD VOLUME; BRAIN FUNCTION; CHILDBIRTH; CONCEPTION; FEEDBACK SYSTEM; FETOPLACENTAL UNIT; HORMONE ACTION; HUMAN; HYPOTHALAMUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INCREASED APPETITE; MATERNAL BEHAVIOR; MATERNAL STRESS; METABOLIC REGULATION; MOTHER FETUS RELATIONSHIP; NERVE CELL MEMBRANE POTENTIAL; NEUROENDOCRINE SYSTEM; NEUROMODULATION; NONHUMAN; PHENOTYPE; PREGNANCY OUTCOME; PRENATAL STRESS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SEX DIFFERENCE; THIRD TRIMESTER PREGNANCY;

ANIMALS; FEMALE; FETAL DEVELOPMENT; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; NEUROSECRETORY SYSTEMS; PITUITARY-ADRENAL SYSTEM; PREGNANCY; PREGNANCY COMPLICATIONS; STRESS, PHYSIOLOGICAL;

EID: 79957855747     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2010.12.023     Document Type: Article

References (170)

1. Abe H., Hidaka N., Kawagoe C., Odagiri K., Watanabe Y., Ikeda T., et al. Prenatal psychological stress causes higher emotionality, depression-like behavior, and elevated activity in the hypothalamo-pituitary-adrenal axis. Neurosci Res 2007, 59:145-151.
2. Atkinson H.C., Waddell B.J. The hypothalamic-pituitary-adrenal axis in rat pregnancy and lactation: circadian variation and interrelationship of plasma adrenocorticotropin and corticosterone. Endocrinology 1995, 136:512-520.
3. Augustine R.A., Ladyman S.R., Grattan D.R. From feeding one to feeding many: hormone-induced changes in bodyweight homeostasis during pregnancy. J Physiol 2008, 586:387-397.
4. Bale T.L., Contarino A., Smith G.W., Chan R., Gold L.H., Sawchenko P.E., et al. Mice deficient for corticotropin-releasing hormone receptor-2 display anxiety-like behaviour and are hypersensitive to stress. Nat Genet 2000, 24:410-414.
5. Bale T.L., Baram T.Z., Brown A.S., Goldstein J.M., Insel T.R., McCarthy M.M., et al. Early life programming and neurodevelopmental disorders. Biol Psychiatry 2010, 68:314-319.
6. Barbaccia M.L., Serra M., Purdy R.H., Biggio G. Stress and neuroactive steroids. Int Rev Neurobiol 2001, 46:243-272.
7. Barbazanges A., Piazza P.V., Le Moal M., Maccari S. Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J Neurosci 1996, 16:3943-3949.
8. Bealer S.L., Armstrong W.E., Crowley W.R. Oxytocin release in magnocellular nuclei: neurochemical mediators and functional significance during gestation. Am J Physiol Regul Integr Comp Physiol 2010, 299:R452-R458.
9. Benediktsson R., Calder A.A., Edwards C.R.W., Seckl J.R. Placental 11β-hydroxysteroid dehydrogenase: a key regulator of fetal glucocorticoid exposure. Clin Endocrinol 1997, 46:161-166.
10. Bjorkqvist K. Social defeat as a stressor in humans. Physiol Behav 2001, 73:435-442.
11. Bosch O.J., Musch W., Bredewold R., Slattery D.A., Neumann I.D. Prenatal stress increases HPA axis activity and impairs maternal care in lactating female offspring: implications for postpartum mood disorder. Psychoneuroendocrinology 2007, 32:267-278.
12. Bradbury M.J., Akana S.F., Dallman M.F. Roles of type I and II corticosteroid receptors in regulation of basal activity in the hypothalamo-pituitary-adrenal axis during the diurnal trough and the peak: evidence for a nonadditive effect of combined receptor occupation. Endocrinology 1994, 134:1286-1296.
13. Britton D.R., Koob G.F., Rivier J., Vale W. Intraventricular corticotropin-releasing factor enhances behavioral effects of novelty. Life Sci 1982, 31:363-367.
14. Brown R.W., Diaz R., Robson A.C., Kotelevtsev Y.V., Mullins J.J., Kaufman M.H., et al. The ontogeny of 11 beta-hydroxysteroid dehydrogenase type 2 and mineralocorticoid receptor gene expression reveal intricate control of glucocorticoid action in development. Endocrinology 1996, 137:794-797.
15. Brunton P.J. Resetting the dynamic range of hypothalamo-pituitary-adrenal axis stress responses through pregnancy. J Neuroendocrinol 2010, 22:1198-1213.
16. Brunton P.J., Russell J.A. Hypothalamic-pituitary-adrenal responses to centrally administered orexin-A are suppressed in pregnant rats. J Neuroendocrinol 2003, 15:633-637.
17. Brunton P.J., Russell J.A. The expectant brain: adapting for motherhood. Nat Rev Neurosci 2008, 9:11-25.
18. Brunton P.J., Russell J.A. Keeping oxytocin neurons under control during stress in pregnancy. Prog Brain Res 2008, 170:365-377.
19. 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.
20. Brunton P.J., Russell J.A. Allopregnanolone and suppressed hypthalamo-pituitary-adenal axis stress responses in late pregnancy in the rat. Stress 2011, 14:6-12.
21. Brunton PJ and Russell JA. Endocrine induced changes in brain function during pregnancy. Brain Res 2010b;1364:198-215.
22. Brunton P.J., Ma S., Shipston M.J., Wigger A., Neumann I.D., Douglas A.J., et al. Central mechanisms underlying reduced ACTH stress responses in pregnant rats: attenuated acute gene activation in the parvocellular paraventricular nucleus (pPVN). Eur J Neurosci 2000, 12:184.17.
23. Brunton P.J., Meddle S.L., Ma S., Ochedalski T., Douglas A.J., Russell J.A. Endogenous opioids and attenuated hypothalamic-pituitary-adrenal axis responses to immune challenge in pregnant rats. J Neurosci 2005, 25:5117-5126.
24. Brunton P.J., Bales J., Russell J.A. Neuroendocrine stress but not feeding responses to centrally administered neuropeptide Y are suppressed in pregnant rats. Endocrinology 2006, 147:3737-3745.
25. Brunton P.J., Sabatier N., Leng G., Russell J.A. Suppressed oxytocin neuron responses to immune challenge in late pregnant rats: a role for endogenous opioids. Eur J Neurosci 2006, 23:1241-1247.
26. Brunton P.J., Arunachalam S., Russell J.A. Control of neurohypophysial hormone secretion, blood osmolality and volume in pregnancy. J Physiol Pharmacol 2008, 59(Suppl. 8):27-45.
27. Brunton P.J., Russell J.A., Douglas A.J. Adaptive responses of the maternal hypothalamic-pituitary-adrenal axis during pregnancy and lactation. J Neuroendocrinol 2008, 20:764-776.
28. Brunton P.J., McKay A.J., Ochedalski T., Piastowska A., Rebas E., Lachowicz A., et al. Central opioid inhibition of neuroendocrine stress responses in pregnancy in the rat is induced by the neurosteroid allopregnanolone. J Neurosci 2009, 29:6449-6460.
29. Burton P.J., Waddell B.J. 11β-Hydroxysteroid dehydrogenase in the rat placenta: developmental changes and the effects of altered glucocorticoid exposure. J Endocrinol 1994, 143:505-513.
30. Burton P.J., Waddell B.J. Dual function of 11β-hydroxysteroid dehydrogenase in placenta: modulating placental glucocorticoid passage and local steroid action. Biol Reprod 1999, 60:234-240.
31. Calvo N., Volosin M. Glucocorticoid and mineralocorticoid receptors are involved in the facilitation of anxiety-like response induced by restraint. Neuroendocrinology 2001, 73:261-271.
32. Clarkson J., Herbison A.E. Oestrogen, kisspeptin, GPR54 and the pre-ovulatory luteinising hormone surge. J Neuroendocrinol 2009, 21:305-311.
33. Concas A., Follesa P., Barbaccia M.L., Purdy R.H., Biggio G. Physiological modulation of GABA(A) receptor plasticity by progesterone metabolites. Eur J Pharmacol 1999, 375:225-235.
34. Cratty M.S., Ward H.E., Johnson E.A., Azzaro A.J., Birkle D.L. Prenatal stress increases corticotropin-releasing factor (CRF) content and release in rat amygdala minces. Brain Res 1995, 675:297-302.
35. da Costa AP, Wood S, Ingram CD, Lightman SL Region-specific reduction in stress-induced c-fos mRNA expression during pregnancy and lactation. Brain Res 1996, 742:177-184.
36. Dallman M.F., Akana S.F., Bhatnagar S., Bell M.E., Choi S., Chu A., et al. Starvation: early signals, sensors, and sequelae. Endocrinology 1999, 140:4015-4023.
37. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 2008, 9:46-56.
38. de Kloet E.R., Vreugdenhil E., Oitzl M.S., Joëls M. Brain corticosteroid receptor balance in health and disease. Endocr Rev 1998, 19:269-301.
39. de Kloet E.R., Joëls M., Holsboer F. Stress and the brain: from adaptation to disease. Nat Rev Neurosci 2005, 6:463-475.
40. de Kloet E.R., Fitzsimons C.P., Datson N.A., Meijer O.C., Vreugdenhil E. Glucocorticoid signaling and stress-related limbic susceptibility pathway: about receptors, transcription machinery and microRNA. Brain Res 2009, 1293:129-141.
41. Devorshak-Harvey E., Bona-Gallo A., Gallo R.V. Endogenous opioid peptide regulation of pulsatile luteinizing hormone secretion during pregnancy in the rat. Neuroendocrinology 1987, 46:369-378.
42. Di S., Malcher-Lopes R., Halmos K.C., Tasker J.G. Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J Neurosci 2003, 23:4850-4857.
43. Diaz R., Brown R.W., Seckl J.R. Distinct ontogeny of glucocorticoid and mineralocorticoid receptor and 11beta-hydroxysteroid dehydrogenase types I and II mRNAs in the fetal rat brain suggest a complex control of glucocorticoid actions. J Neurosci 1998, 18:2570-2580.
44. Douglas A.J. Mother-offspring dialogue in early pregnancy: impact of adverse environment on pregnancy maintenance and neurobiology. Prog Neuropsychopharmacol Biol Psychiatry 2010, [Aug 3. Epub ahead of print PMID: 20688125].
45. Douglas A.J. Baby on board: do responses to stress in the maternal brain mediate adverse pregnancy outcome?. Front Neuroendocrinol 2010, 31:359-376.
46. Douglas A.J., Neumann I., Meeren H.K., Leng G., Johnstone L.E., Munro G., Russell J.A. Central endogenous opioid inhibition of supraoptic oxytocin neurons in pregnant rats. J Neurosci 1995, 15:5049-5057.
47. Douglas A.J., Johnstone H.A., Wigger A., Landgraf R., Russell J.A., Neumann I.D. The role of endogenous opioids in neurohypophysial and hypothalamo-pituitary-adrenal axis hormone secretory responses to stress in pregnant rats. J Endocrinol 1998, 158:285-293.
48. Douglas A.J., Johnstone H., Brunton P., Russell J.A. Sex-steroid induction of endogenous opioid inhibition on oxytocin secretory responses to stress. J Neuroendocrinol 2000, 12:343-350.
49. Douglas A.J., Johnstone L.E., Leng G. Neuroendocrine mechanisms of change in food intake during pregnancy: a potential role for brain oxytocin. Physiol Behav 2007, 91:352-365.
50. Droste S.K., de Groote L., Lightman S.L., Reul J.M., Linthorst A.C. The ultradian and circadian rhythms of free corticosterone in the brain are not affected by gender: an in vivo microdialysis study in Wistar rats. J Neuroendocrinol 2009, 21:132-140.
51. Dunn A.J., Berridge C.W. Physiological and behavioral responses to corticotropin-releasing factor administration: is CRF a mediator of anxiety or stress responses?. Brain Res Rev 1990, 15:71-100.
52. Dunn G.A., Morgan C.P., Bale T.L. Sex-specificity in transgenerational epigenetic programming. Horm Behav 2010, [Epub ahead of print].
53. Dunn E., Kapoor A., Leen J., Matthews S.G. Prenatal synthetic glucocorticoid exposure alters hypothalamic-pituitary-adrenal regulation and pregnancy outcomes in mature female guinea pigs. J Physiol 2010, 588:887-899.
54. Ericsson A., Kovacs K.J., Sawchenko P.E. A functional anatomical analysis of central pathways subserving the effects of interleukin-1 on stress-related neuroendocrine neurons. J Neurosci 1994, 14:897-913.
55. Estanislau C., Morato S. Behavior ontogeny in the elevated plus-maze: prenatal stress effects. Int J Dev Neurosci 2006, 24:255-262.
56. Evanson N.K., Tasker J.G., Hill M.N., Hillard C.J., Herman J.P. Fast feedback inhibition of the HPA axis by glucocorticoids is mediated by endocannabinoid signaling. Endocrinology 2010, 151:4811-4819.
57. Fan J.M., Chen X.Q., Jin H., Du J.Z. Gestational hypoxia alone or combined with restraint sensitizes the hypothalamic-pituitary-adrenal axis and induces anxiety-like behavior in adult male rat offspring. Neuroscience 2009, 159:1363-1373.
58. Fride E., Dan Y., Feldon J., Halevy G., Weinstock M. Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats. Physiol Behav 1986, 37:681-687.
59. Frye C.A., Orecki Z.A. Prenatal stress produces deficits in socio-sexual behavior of cycling, but not hormone-primed, Long-Evans rats. Pharmacol Biochem Behav 2002, 73:53-60.
60. Gotoh K., Fukagawa K., Fukagawa T., Noguchi H., Kakuma T., Sakata T., et al. Glucagon-like peptide-1, corticotropin-releasing hormone, and hypothalamic neuronal histamine interact in the leptin-signaling pathway to regulate feeding behavior. FASEB J 2005, 19:1131-1133.
61. 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.
62. Handa R.J., Weiser M.J., Zuloaga D.G. A role for the androgen metabolite, 5alpha-androstane-3beta, 17beta-diol, in modulating oestrogen receptor beta-mediated regulation of hormonal stress reactivity. J Neuroendocrinol 2009, 21:351-358.
63. Hellemans K.G., Verma P., Yoon E., Yu W.K., Young A.H., Weinberg J. Prenatal alcohol exposure and chronic mild stress differentially alter depressive- and anxiety-like behaviors in male and female offspring. Alcohol Clin Exp Res 2010, 34:633-645.
64. Heller C.L., Orti E., De Nicola A.F. Regulatory factors of glucocorticoid binding in early and term rat placenta. J Steroid Biochem 1986, 25:53-58.
65. Henry C., Kabbaj M., Simon H., Le Moal M., Maccari S. Prenatal stress increases the hypothalamo-pituitary-adrenal axis response in young and adult rats. J Neuroendocrinol 1994, 6:341-345.
66. Herman J.P., Figueiredo H., Mueller N.K., Ulrich-Lai Y., Ostrander M.M., Choi D.C., et al. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 2003, 24:151-180.
67. Holmes M.C., Abrahamsen C.T., French K.L., Paterson J.M., Mullins J.J., Seckl J.R. 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.
68. Holson R.R., Gough B., Sullivan P., Badger T., Sheehan D.M. Prenatal dexamethasone or stress but not ACTH or corticosterone alter sexual behavior in male rats. Neurotoxicol Teratol 1995, 17:393-401.
69. Hsu D.T., Chen F.L., Takahashi L.K., Kalin N.H. Rapid stress-induced elevations in corticotropin-releasing hormone mRNA in rat central amygdala nucleus and hypothalamic paraventricular nucleus: an in situ hybridization analysis. Brain Res 1998, 788:305-310.
70. Igosheva N., Klimova O., Anishchenko T., Glover V. Prenatal stress alters cardiovascular responses in adult rats. J Physiol 2004, 557:273-285.
71. Jankord R., Herman J.P. Limbic regulation of hypothalamo-pituitary-adrenocortical function during acute and chronic stress. Ann NY Acad Sci 2008, 1148:64-73.
72. Jin Y., Penning T.M. Steroid 5alpha-reductases and 3alpha-hydroxysteroid dehydrogenases: key enzymes in androgen metabolism. Best Pract Res Clin Endocrinol Metab 2001, 15:79-94.
73. Joachim R., Zenclussen A.C., Polgar B., Douglas A.J., Fest S., Knackstedt M., et al. The progesterone derivative dydrogesterone abrogates murine stress-triggered abortion by inducing a Th2 biased local immune response. Steroids 2003, 68:931-940.
74. Joëls M., Karst H., DeRijk R., de Kloet E.R. The coming out of the brain mineralocorticoid receptor. Trends Neurosci 2008, 31:1-7.
75. Johnstone H.A., Wigger A., Douglas A.J., Neumann I.D., Landgraf R., Seckl J.R., et al. Attenuation of hypothalamic-pituitary-adrenal axis stress responses in late pregnancy: changes in feedforward and feedback mechanisms. J Neuroendocrinol 2000, 12:811-822.
76. Kalabis G.M., Kostaki A., Andrews M.H., Petropoulos S., Gibb W., Matthews S.G. Multidrug resistance phosphoglycoprotein (ABCB1) in the mouse placenta: fetal protection. Biol Reprod 2005, 73:591-597.
77. Kappeler L., Meaney M.J. Epigenetics and parental effects. Bioessays 2010, 32:818-827.
78. Karst H., Berger S., Turiault M., Tronche F., Schütz G., Joëls M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc Natl Acad Sci USA 2005, 102:19204-19207.
79. Karst H., Berger S., Erdmann G., Schütz G., Joëls M. Metaplasticity of amygdalar responses to the stress hormone corticosterone. Proc Natl Acad Sci USA 2010, 07:14449-14454.
80. Keverne E.B. Epigenetically regulated imprinted genes and foetal programming. Neurotox Res 2010, 18:386-392.
81. Kleinhaus K., Steinfeld S., Balaban J., Goodman L., Craft T.S., Malaspina D., et al. Effects of excessive glucocorticoid receptor stimulation during early gestation on psychomotor and social behavior in the rat. Dev Psychobiol 2010, 52:121-132.
82. Koehl M., Barbazanges A., Le Moal M., Maccari S. Prenatal stress induces a phase advance of circadian corticosterone rhythm in adult rats which is prevented by postnatal stress. Brain Res 1997, 759:317-320.
83. Koehl M., Darnaudery M., Dulluc J., Van Reeth O., Le Moal M., Maccari S. Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both gender. J Neurobiol 1999, 40:302-315.
84. Koenig J.I., Elmer G.I., Shepard P.D., Lee P.R., Mayo C., Joy B., et al. Prenatal exposure to a repeated variable stress paradigm elicits behavioral and neuroendocrinological changes in the adult offspring: potential relevance to schizophrenia. Behav Brain Res 2005, 156:251-261.
85. Koksma J.J., van Kesteren R.E., Rosahl T.W., Zwart R., Smit A.B., Lüddens H., et al. Oxytocin regulates neurosteroid modulation of GABA(A) receptors in supraoptic nucleus around parturition. J Neurosci 2003, 23:788-797.
86. la Fleur S.E., Akana S.F., Manalo S.L., Dallman M.F. Interaction between corticosterone and insulin in obesity: regulation of lard intake and fat stores. Endocrinology 2004, 145:2174-2185.
87. Ladyman S.R., Tups A., Augustine R.A., Swahn-Azavedo A., Kokay I.C., Grattan D.R. Loss of hypothalamic response to leptin during pregnancy associated with development of melanocortin resistance. J Neuroendocrinol 2009, 21:449-456.
88. Ladyman S.R., Augustine R.A., Grattan D.R. Hormone interactions regulating energy balance during pregnancy. J Neuroendocrinol 2010, 22:805-817.
89. Lambert J.J., Cooper M.A., Simmons R.D., Weir C.J., Belelli D. Neurosteroids: endogenous allosteric modulators of GABA(A) receptors. Psychoneuroendocrinology 2009, 34(Suppl. 1):S48-S58.
90. Laugero K.D., Gomez F., Manalo S., Dallman M.F. Corticosterone infused intracerebroventricularly inhibits energy storage and stimulates the hypothalamo-pituitary axis in adrenalectomized rats drinking sucrose. Endocrinology 2002, 143:4552-4562.
91. Lee Y., Voogt J.L. Feedback effects of placental lactogens on prolactin levels and Fos-related antigen immunoreactivity of tuberoinfundibular dopaminergic neurons in the arcuate nucleus during pregnancy in the rat. Endocrinology 1999, 140:2159-2166.
92. Lemaire V., Koehl M., Le Moal M., Abrous D.N. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 2000, 97:11032-11037.
93. Lemberger T., Staels B., Saladin R., Desvergne B., Auwerx J., Wahli W. Regulation of the peroxisome proliferator-activated receptor alpha gene by glucocorticoids. J Biol Chem 1994, 269:24527-24530.
94. Lesage J., Sebaai N., Leonhardt M., Dutriez-Casteloot I., Breton C., Deloof S., et al. Perinatal maternal undernutrition programs the offspring hypothalamo-pituitary-adrenal (HPA) axis. Stress 2006, 9:183-198.
95. Levay E.A., Paolini A.G., Govic A., Hazi A., Penman J., Kent S. Anxiety-like behaviour in adult rats perinatally exposed to maternal calorie restriction. Behav Brain Res 2008, 191:164-172.
96. Lucassen P.J., Bosch O.J., Jousma E., Krömer S.A., Andrew R., Seckl J.R., et al. Prenatal stress reduces postnatal neurogenesis in rats selectively bred for high, but not low, anxiety: possible key role of placental 11beta-hydroxysteroid dehydrogenase type 2. Eur J Neurosci 2009, 29:97-103.
97. Ma S., Shipston M.J., Morilak D., Russell J.A. Reduced hypothalamic vasopressin secretion underlies attenuated adrenocorticotropin stress responses in pregnant rats. Endocrinology 2005, 146:1626-1637.
98. Maccari S., Piazza P.V., Kabbaj M., Barbazanges A., Simon H., Le Moal M. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci 1995, 15:110-116.
99. Mairesse J., Lesage J., Breton C., Bréant B., Hahn T., Darnaudéry M., et al. Maternal stress alters endocrine function of the feto-placental unit in rats. Am J Physiol Endocrinol Metab 2007, 292:E1526-E1533.
100. Makino S., Gold P.W., Schulkin J. Corticosterone effects on corticotropin-releasing hormone mRNA in the central nucleus of the amygdala and the parvocellular region of the paraventricular nucleus of the hypothalamus. Brain Res 1994, 640:105-112.
101. Mann P.E., Bridges R.S. Lactogenic hormone regulation of maternal behavior. Prog Brain Res 2001, 133:251-262.
102. 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.
103. Mark P.J., Augustus S., Lewis J.L., Hewitt D.P., Waddell B.J. Changes in the placental glucocorticoid barrier during rat pregnancy: impact on placental corticosterone levels and regulation by progesterone. Biol Reprod 2009, 80:1209-1215.
104. Matthews S.G. Early programming of the hypothalamo-pituitary-adrenal axis. Trends Endocrinol Metab 2002, 13:373-380.
105. Matthews S.G., Owen D., Banjanin S., Andrews M.H. Glucocorticoids, hypothalamo-pituitary-adrenal (HPA) development, and life after birth. Endocr Res 2002, 28:709-718.
106. McCarthy M.M., Auger A.P., Bale T.L., De Vries G.J., Dunn G.A., Forger N.G., et al. The epigenetics of sex differences in the brain. J Neurosci 2009, 29:12815-12823.
107. 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. Dev Brain Res 1995, 84:55-61.
108. McEwen B.S. Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol 2008, 583:174-185.
109. Meaney M.J. Epigenetics and the biological definition of gene-environment interactions. Child Dev 2010, 81:41-79.
110. Meaney M.J., Szyf M., Seckl J.R. Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Mol Med 2007, 13:269-277.
111. Morley-Fletcher S., Rea M., Maccari S., Laviola G. Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. Eur J Neurosci 2003, 18:3367-3374.
112. Morley-Fletcher S., Darnaudery M., Mocaer E., Froger N., Lanfumey L., Laviola G., et al. Chronic treatment with imipramine reverses immobility behaviour, hippocampal corticosteroid receptors and cortical 5-HT(1A) receptor mRNA in prenatally stressed rats. Neuropharmacology 2004, 47:841-847.
113. Mueller B.R., Bale T.L. Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 2008, 28:9055-9065.
114. Murgatroyd C., Patchev A.V., Wu Y., Micale V., Bockmuhl Y., Fischer D., et al. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 2009, 12:1559-1566.
115. Neumann I.D., Johnstone H.A., Hatzinger M., Liebsch G., Shipston M., Russell J.A., et al. Attenuated neuroendocrine responses to emotional and physical stressors in pregnant rats involve adenohypophysial changes. J Physiol 1998, 508:289-300.
116. Nilsson C., Larsson B.M., Jennische E., Eriksson E., Bjorntorp P., York D.A., et al. Maternal endotoxemia results in obesity and insulin resistance in adult male offspring. Endocrinology 2001, 142:2622-2630.
117. Oitzl M.S., Champagne D.L., van der Veen R., de Kloet E.R. Brain development under stress: hypotheses of glucocorticoid actions revisited. Neurosci Biobehav Rev 2010, 34:853-866.
118. Olijslagers J.E., de Kloet E.R., Elgersma Y., van Woerden G.M., Joëls M., Karst H. Rapid changes in hippocampal CA1 pyramidal cell function via pre- as well as postsynaptic membrane mineralocorticoid receptors. Eur J Neurosci 2008, 27:2542-2550.
119. Ondrejcakova M., Bakos J., Garafova A., Kovacs L., Kvetnansky R., Jezova D. Neuroendocrine and cardiovascular parameters during simulation of stress-induced rise in circulating oxytocin in the rat. Stress 2010, 13:314-322.
120. Pankevich D.E., Mueller B.R., Brockel B., Bale T.L. Prenatal stress programming of offspring feeding behavior and energy balance begins early in pregnancy. Physiol Behav 2009, 98:94-102.
121. Parker V.J., Douglas A.J. Stress in early pregnancy: maternal neuroendocrine-immune responses and effects. Am J Immunol 2010, 85:86-92.
122. Pedersen C.A., Boccia M.L. Oxytocin links mothering received, mothering bestowed and adult stress responses. Stress 2002, 5:259-267.
123. Peters D.A.V. Prenatal stress: effects on brain biogenic amine and plasma corticosterone levels. Pharmacol Biochem Behav 1982, 17:721-725.
124. Poletini M.O., Szawka R.E., Franci C.R., Anselmo-Franci J.A. Ovarian steroids but not the locus coeruleus regulate stress-induced prolactin secretion in female rats. J Neuroendocrinol 2006, 18:938-948.
125. Poltyrev T., Keshet G.I., Kay G., Weinstock M. Role of experimental conditions in determining differences in exploratory behavior of prenatally stressed rats. Dev Psychobiol 1996, 29:453-462.
126. Poltyrev T., Gorodetsky E., Bejar C., Schorer-Apelbaum D., Weinstock M. Effect of chronic treatment with ladostigil (TV-3326) on anxiogenic and depressive-like behaviour and on activity of the hypothalamic-pituitary-adrenal axis in male and female prenatally stressed rats. Psychopharmacology Berl 2005, 181:118-125.
127. Pruett S.B. Quantitative aspects of stress-induced immunomodulation. Int Immunopharmacol 2001, 1:507-520.
128. Puia G., Santi M.R., Vicini S., Pritchett D.B., Purdy R.H., Paul S.M., et al. Neurosteroids act on recombinant human GABAA receptors. Neuron 1990, 4:759-765.
129. Purdy R.H., Morrow A.L., Moore P.H., Paul S.M. Stress-induced elevations of gamma-aminobutyric acid type A receptor-active steroids in the rat brain. Proc Natl Acad Sci USA 1991, 88:4553-4557.
130. Reddy D.S., Jian K. The testosterone-derived neurosteroid androstanediol is a positive allosteric modulator of GABAA receptors. J Pharmacol Exp Ther 2010, 334:1031-1041.
131. Roa J., Vigo E., Castellano J.M., Navarro V.M., Fernández-Fernández R., Casanueva F.F., et al. Hypothalamic expression of KiSS-1 system and gonadotropin-releasing effects of kisspeptin in different reproductive states of the female rat. Endocrinology 2006, 1472864-1472878.
132. Rosenblatt J.S., Mayer A.D., Giordano A.L. Hormonal basis during pregnancy for the onset of maternal behavior in the rat. Psychoneuroendocrinology 1988, 13:29-46.
133. Rossoni E., Feng J., Tirozzi B., Brown D., Leng G., Moos F. Emergent synchronous bursting of oxytocin neuronal network. PLoS Comput Biol 2008, 18(4(7)):e1000123.
134. Russell JA, Brunton PJ. Bringing forth the next generation. and the next. In: Neurobiology of the Parental Brain, ed. RS Bridges, Academic Press 2008;13, 203-23.
135. Russell J.A., Leng G., Douglas A.J. The magnocellular oxytocin system, the fount of maternity: adaptations in pregnancy. Front Neuroendocrinol 2003, 24:27-61.
136. Schulkin J., Gold P.W., McEwen B.S. Induction of corticotropin-releasing hormone gene expression by glucocorticoids: implication for understanding the states of fear and anxiety and allostatic load. Psychoneuroendocrinology 1998, 23:219-243.
137. Seckl J.R., Meaney M.J. Glucocorticoid programming. Ann NY Acad Sci 2004, 1032:63-84.
138. Shahrokh D.K., Zhang T.Y., Diorio J., Gratton A., Meaney M.J. Oxytocin-dopamine interactions mediate variations in maternal behavior in the rat. Endocrinology 2010, 151:2276-2286.
139. Sherwood O.D., Crnekovic V.E., Gordon W.L., Rutherford J.E. Radioimmunoassay of relaxin throughout pregnancy and during parturition in the rat. Endocrinology 1980, 107:691-698.
140. Shoener J.A., Baig R., Page K.C. Prenatal exposure to dexamethasone alters hippocampal drive on hypothalamic-pituitary-adrenal axis activity in adult male rats. Am J Physiol Regul Integr Comp Physiol 2006, 290:R1366-R1373.
141. Soares M.J., Müller H., Orwig K.E., Peters T.J., Dai G. The uteroplacental prolactin family and pregnancy. Biol Reprod 1998, 58:273-284.
142. Somponpun S.J., Holmes M.C., Seckl J.R., Russell J.A. Modulation of oestrogen receptor-beta mRNA expression in rat paraventricular and supraoptic nucleus neurones following adrenal steroid manipulation and hyperosmotic stimulation. J Neuroendocrinol 2004, 16:472-482.
143. Speirs H.J., Seckl J.R., Brown R.W. Ontogeny of glucocorticoid receptor and 11beta-hydroxysteroid dehydrogenase type-1 gene expression identifies potential critical periods of glucocorticoid susceptibility during development. J Endocrinol 2004, 181:105-116.
144. Sunn N., Egli M., Burazin T.C., Burns P., Colvill L., Davern P., et al. Circulating relaxin acts on subfornical organ neurons to stimulate water drinking in the rat. Proc Natl Acad Sci USA 2002, 99:1701-1706.
145. Szuran T.F., Pliska V., Pokorny J., Welzl H. Prenatal stress in rats: effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance. Physiol Behav 2000, 71:353-362.
146. Szyf M., Weaver I.C., Champagne F.A., Diorio J., Meaney M.J. Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Front Neuroendocrinol 2005, 26:139-162.
147. Takahashi L.K., Kalin N.H. Early developmental and temporal characteristics of stress-induced secretion of pituitary-adrenal hormones in prenatally stressed rat pups. Brain Res 1991, 558:75-78.
148. Takahashi L.K., Turner J.G., Kalin N.H. Prolonged stress-induced elevation in plasma corticosterone during pregnancy in the rat: implications for prenatal stress studies. Psychoneuroendocrinology 1998, 23:571-581.
149. Tamashiro K.L., Terrillion C.E., Hyun J., Koenig J.I., Moran T.H. Prenatal stress or high-fat diet increases susceptibility to diet-induced obesity in rat offspring. Diabetes 2009, 58:1116-1125.
150. Tian L., Philp J.A., Shipston M.J. Glucocorticoid block of protein kinase C signalling in mouse pituitary corticotroph AtT20 D16:16 cells. J Physiol 1999, 516:757-768.
151. Ulrich-Lai Y.M., Herman J.P. Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 2009, 10:397-409.
152. 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.
153. Waddell B.J., Benediktsson R., Brown R.W., Seckl J.R. Tissue-specific messenger ribonucleic acid expression of 11beta-hydroxysteroid dehydrogenase types 1 and 2 and the glucocorticoid receptor within rat placenta suggests exquisite local control of glucocorticoid action. Endocrinology 1998, 139:1517-1523.
154. Wakshlak A., Weinstock M. Neonatal handling reverses behavioral abnormalities induced in rats by prenatal stress. Physiol Behav 1990, 48:289-292.
155. Walf A.A., Frye C.A. Estradiol decreases anxiety behavior and enhances inhibitory avoidance and gestational stress produces opposite effects. Stress 2007, 10:251-260.
156. Wartella J., Amory E., Lomas L.M., Macbeth A., McNamara I., Stevens L., et al. Single or multiple reproductive experiences attenuate neurobehavioral stress and fear responses in the female rat. Physiol Behav 2003, 79:373-381.
157. Weinstock M. The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav Immun 2005, 19:296-308.
158. Weinstock M. Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 2007, 32:1730-1740.
159. Weinstock M., Matlina E., Maor G.I., Rosen H., McEwen B.S. Prenatal stress selectivity alters the reactivity of the hypothalamic-pituitary adrenal system in the female rat. Brain Res 1992, 595:195-200.
160. Weiser M.J., Handa R.J. Estrogen impairs glucocorticoid dependent negative feedback on the hypothalamic-pituitary-adrenal axis via estrogen receptor alpha within the hypothalamus. Neuroscience 2009, 159:883-895.
161. Welberg L.A., Seckl J.R., Holmes M.C. 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 2000, 12:1047-1054.
162. Welberg L.A., Thrivikraman K.V., Plotsky P.M. Chronic maternal stress inhibits the capacity to up-regulate placental 11beta-hydroxysteroid dehydrogenase type 2 activity. J Endocrinol 2005, 186:R7-R12.
163. Wigger A., Lörscher P., Oehler I., Keck M.E., Naruo T., Neumann I.D. Nonresponsiveness of the rat hypothalamo-pituitary-adrenocortical axis to parturition-related events: inhibitory action of endogenous opioids. Endocrinology 1999, 140:2843-2849.
164. Wilcoxon J.S., Redei E.E. Maternal glucocorticoid deficit affects hypothalamic-pituitary-adrenal function and behavior of rat offspring. Horm Behav 2007, 51:321-327.
165. Williamson M., Viau V. Selective contributions of the medial preoptic nucleus to testosterone-dependant regulation of the paraventricular nucleus of the hypothalamus and the HPA axis. Am J Physiol Regul Integr Comp Physiol 2008, 295:R1020-R1030.
166. Williamson M., Bingham B., Gray M., Innala L., Viau V. The medial preoptic nucleus integrates the central influences of testosterone on the paraventricular nucleus of the hypothalamus and its extended circuitries. J Neurosci 2010, 30:11762-11770.
167. Yaka R., Salomon S., Matzner H., Weinstock M. Effect of varied gestational stress on acquisition of spatial memory, hippocampal LTP and synaptic proteins in juvenile male rats. Behav Brain Res 2007, 179:126-132.
168. 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.
169. Zhang J., Rivest S. Distribution, regulation and colocalization of the genes encoding the EP2- and EP4-PGE2 receptors in the rat brain and neuronal responses to systemic inflammation. Eur J Neurosci 1999, 11:2651-2668.
170. Zuena A.R., Mairesse J., Casolini P., Cinque C., Alema G.S., Morley-Fletcher S., et al. Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLoS ONE 2008, 3:e2170.