Differential adaptive responses to chronic stress of maternally stressed male mice offspring.

It is well established that stress in early life can alter the activity of the hypothalamus-pituitary-adrenal (HPA) axis, but most studies to date have focused on HPA reactivity in response to a single acute stress. The present study addressed whether stress in pregnant mice could influence the adaptive responses of their offspring to chronic stress. Male offspring were exclusively used in this study. Elevated plus maze tests revealed that 14 d of repeated restraint stress (6 h per day; from postnatal d 50-63) significantly increased anxiety-like behavior in maternally stressed mice. NBI 27914, a CRH receptor antagonist, completely eliminated anxiety-related behaviors in a dose-dependent manner, indicating an involvement of a hyperactive CRH system. In accordance with increased anxiety, CRH contents in the hypothalamus and amygdala were significantly higher in these mice. Despite an increased basal activity of the CRH-ACTH system, the combination of chronic prenatal and postnatal stress resulted in a significant reduction of basal plasma corticosterone level, presumably because of a defect in adrenal function. Along with alterations in hypothalamic and hippocampal corticosteroid receptors, it was also demonstrated that a dysfunction in negative feedback inhibition of the HPA axis could be deteriorated by chronic stress in maternally stressed male mice. Taken together, these results indicate that exposure to maternal stress in the womb can affect an animal's coping capacity to chronic postnatal stress.

[1]  Hosung Jung,et al.  Excision of the First Intron from the Gonadotropin-releasing Hormone (GnRH) Transcript Serves as a Key Regulatory Step for GnRH Biosynthesis* , 2003, The Journal of Biological Chemistry.

[2]  S. D. de Boer,et al.  A robust animal model of state anxiety: fear-potentiated behaviour in the elevated plus-maze. , 2003, European journal of pharmacology.

[3]  P. Hof,et al.  Repeated restraint stress suppresses neurogenesis and induces biphasic PSA‐NCAM expression in the adult rat dentate gyrus , 2003, The European journal of neuroscience.

[4]  J. Palermo-neto,et al.  Effects of prenatal stress on stress-induced changes in behavior and macrophage activity of mice , 2002, Physiology & Behavior.

[5]  S. Chattarji,et al.  Chronic Stress Induces Contrasting Patterns of Dendritic Remodeling in Hippocampal and Amygdaloid Neurons , 2002, The Journal of Neuroscience.

[6]  N. Kalin,et al.  Reduction of Stress-Induced Behavior by Antagonism of Corticotropin-Releasing Hormone 2 (CRH2) Receptors in Lateral Septum or CRH1 Receptors in Amygdala , 2002, The Journal of Neuroscience.

[7]  J. D. McGaugh,et al.  Role of adrenal stress hormones in forming lasting memories in the brain , 2002, Current Opinion in Neurobiology.

[8]  George Paxinos,et al.  The Mouse Brain in Stereotaxic Coordinates , 2001 .

[9]  M. Mattson,et al.  Impact of aging on stress-responsive neuroendocrine systems , 2001, Mechanisms of Ageing and Development.

[10]  J. Seckl,et al.  Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour , 2001, Neuroscience.

[11]  M. Volosin,et al.  Glucocorticoid and Mineralocorticoid Receptors Are Involved in the Facilitation of Anxiety-Like Response Induced by Restraint , 2001, Neuroendocrinology.

[12]  K. Barron,et al.  Corticosterone delivery to the amygdala increases corticotropin-releasing factor mRNA in the central amygdaloid nucleus and anxiety-like behavior , 2000, Brain Research.

[13]  J. Seckl,et al.  Inhibition of 11β‐hydroxysteroid dehydrogenase, the foeto‐placental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxiety‐like behaviour in the offspring , 2000, The European journal of neuroscience.

[14]  B. McEwen Allostasis and Allostatic Load: Implications for Neuropsychopharmacology , 2000, Neuropsychopharmacology.

[15]  Joseph E LeDoux,et al.  Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. , 1999, Behavioral neuroscience.

[16]  M. Moal,et al.  Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both gender. , 1999, Journal of neurobiology.

[17]  R. Rubin,et al.  Functional sex differences (`sexual diergism') of central nervous system cholinergic systems, vasopressin, and hypothalamic–pituitary–adrenal axis activity in mammals: a selective review , 1999, Brain Research Reviews.

[18]  B. McEwen,et al.  Support for a Bimodal Role for Type II Adrenal Steroid Receptors in Spatial Memory , 1999, Neurobiology of Learning and Memory.

[19]  M. Joëls,et al.  Brain corticosteroid receptor balance in health and disease. , 1998, Endocrine reviews.

[20]  T. Baram,et al.  The CRF1 receptor mediates the excitatory actions of corticotropin releasing factor (CRF) in the developing rat brain: in vivo evidence using a novel, selective, non-peptide CRF receptor antagonist , 1997, Brain Research.

[21]  M. Le Moal,et al.  Prenatal Stress Induces High Anxiety and Postnatal Handling Induces Low Anxiety in Adult Offspring: Correlation with Stress-Induced Corticosterone Secretion , 1997, The Journal of Neuroscience.

[22]  J. Herman,et al.  Neurocircuitry of stress: central control of the hypothalamo–pituitary–adrenocortical axis , 1997, Trends in Neurosciences.

[23]  M. Le Moal,et al.  Maternal Glucocorticoid Secretion Mediates Long-Term Effects of Prenatal Stress , 1996, The Journal of Neuroscience.

[24]  Richard F. Thompson,et al.  Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[25]  C. Stratakis,et al.  Neuroendocrinology and Pathophysiology of the Stress System , 1995, Annals of the New York Academy of Sciences.

[26]  B. McEwen,et al.  Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: Comparison of stressors , 1995, Neuroscience.

[27]  Shakti Sharma,et al.  Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. , 1995, Brain research. Developmental brain research.

[28]  M. Le Moal,et al.  Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  H. Simon,et al.  Prenatal Stress Increases the Hypothalamo‐Pituitary‐Adrenal Axis Response in Young and Adult Rats , 1994, Journal of neuroendocrinology.

[30]  J. Schulkin,et al.  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 , 1994, Brain Research.

[31]  Bruce S. McEwen,et al.  Repeated stress causes reversible impairments of spatial memory performance , 1994, Brain Research.

[32]  N. Kalin,et al.  Attenuation of stress-induced behavior by antagonism of corticotropin-releasing factor receptors in the central amygdala in the rat , 1993, Brain Research.

[33]  B. McEwen,et al.  Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary adrenal system in the female rat , 1992, Brain Research.

[34]  Bruce S. McEwen,et al.  Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons , 1992, Brain Research.

[35]  M. Joëls,et al.  Control of neuronal excitability by corticosteroid hormones , 1992, Trends in Neurosciences.

[36]  N. Kalin,et al.  Stressor controllability during pregnancy influences pituitary-adrenal hormone concentrations and analgesic responsiveness in offspring , 1988, Physiology & Behavior.

[37]  K. Kovács,et al.  Dexamethasone inhibits corticotropin-releasing factor gene expression in the rat paraventricular nucleus. , 1987, Neuroendocrinology.

[38]  P. Sawchenko Evidence for a local site of action for glucocorticoids in inhibiting CRF and vasopressin expression in the paraventricular nucleus , 1987, Brain Research.

[39]  J. Feldon,et al.  Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats , 1986, Physiology & Behavior.

[40]  L. Frohman,et al.  Involvement of hypothalamic somatostatin in the suppression of growth hormone secretion by central corticotropin-releasing factor in conscious male rats. , 1985, Neuroendocrinology.

[41]  J. Martin,et al.  Inhibitory effect of somatostatin (SRIF) on the release of growth hormone (GH) induced in the rat by electrical stimulation. , 1974, Endocrinology.

[42]  K. Montgomery,et al.  The relation between fear induced by novel stimulation and exploratory drive. , 1955 .

[43]  R. Sapolsky Chapter 2 Glucocorticoids, hippocampal damage and the glutamatergic synapse , 1990 .

[44]  F. Kimura,et al.  Effects of intracerebroventricular administration of growth hormone-releasing factor and corticotropin-releasing factor on somatostatin secretion into rat hypophysial portal blood. , 1990, Neuroendocrinology.

[45]  B. Burguera,et al.  Dual and selective actions of glucocorticoids upon basal and stimulated growth hormone release in man. , 1990, Neuroendocrinology.