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Stress
The International Journal on the Biology of Stress
Volume 4, 2001 - Issue 3
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Original Article

Hormonal and Behavioural Abnormalities Induced by Stress in utero: an Animal Model for Depression

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Pages 169-181 | Received 10 Nov 2000, Published online: 07 Jul 2009

References

  • Adrien J., Dugovic C., Martin P. “Sleep-wakefulness patterns in the helpless rat”,. Physiol. Behav 1991; 49: 257–262
  • 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
  • Alonso S J., Navarro E., Santana C., Rodriguez M. “Motor lateralization, behavioral despair and dopaminergic brain asymmetry after prenatal stress”,. Pharmacol. Biochem. Behav 1997; 58: 443–448
  • Alonso S J., Castellano M A., Quintero M., Navarro E. “Action of antidepressant drugs on maternal stress-induced hypoactivity in female rats”,. Meth. Find. Exp. Clin. Pharmacol 1999; 21: 291–295
  • Arendt J. “The pineal gland: basic physiology and clinical implications”,. Endocrinology3rd ed, L J. Degroot. Chapman & Hall, London 1995; 432–444
  • Barbazanges M., Piazza P. V., Le Moal M., Maccari S. “Maternal glucocorticoid secretion mediates long-term effects of prenatal stress”,. J. Neurosci 1996; 16: 7783–7790
  • Barker DJ. “The fetal origins of adult disease”,. Proc. R. Soc. Lond. B Biol. Sci 1995; 262: 37–43
  • Becker G., Kowall M. “Crucial role of the postnatal maternal environment in the expression of prenatal stress effects in the male rats”,. J. Comp. Physiol. Psychol 1977; 91: 432–1446
  • Beck-Friis J., Ljundgren J G., Thoren M., von Rosen D., Kjellman B F., Wetterberg L. “Melatonin, cortisol and ACTH in patients with major depressive disorder and healthy humans with special reference to the outcome of the dexamethasone suppression test”,. Psychoneuroendocrinology 1985; 10: 173–186
  • Bell R W., Nitschke W., Gorry T H., Zachman T A. “Infantile stimulation and ultrasonic signaling: a possible mediator of early handling phenomena”,. Dev Psychobiol 1971; 4: 181–191
  • Besedovsky H O., Sorkin E., Keller M., Muller J. “Change in blood hormone levels during the immune response (39057)”,. Proc. Soc. Exp. Biol. Med 1975; 150: 466–470
  • Cespuglio R., Marinesco S., Baubet V., Bonnet C., El Kafi B. “Evidence for a sleep-promoting influence of stress”,. Adv. Neuroimmunol 1995; 5: 145–154
  • Chapman R., Stern J. “Failure of severe maternal stress or ACTH during pregnancy to affect emotionality of male rat offspring: implications of litter effects for prenatal studies”,. Dev. Psychobiol 1979; 12: 255–269
  • Cheeta S., Ruigt G., van Proosdij J., Willner P. “Changes in sleep architecture after chronic mild stress”,. Biol. Psychiatr 1997; 41: 419–427
  • Dahlof L G., Hard E., Larsson K. “Influence of maternal stress on the development of the fetal genital system”,. Physiol. Behav 1978; 20: 193–195
  • Damaudery M., Buee L., Viltart O., Maccari S. “Chronic stress during pregnancy increases anxiety of female rats”,. 30th Meeting of the American Society for Neuwscience, New Orleans, USA. 2000
  • Day J C., Koehl M., Deroche V., Le Moal M., Maccari S. “Prenatal stress enhances stress-and corticotropin-releasing factor-induced stimulation of hippocampal acetyl-choline release in adult rats”,. J. Neurosci 1998; 18: 1886–1892
  • Delbende C, Tranchand Bunel D., Tarozzo G., Grino M., Oliver C, Mocaër E., Vaudry H. “Effect of chronic treatment with the antidepressant tianeptine on the hypotha-lamo-pituitary-adrenal axis”,. Eur. J. Pharmacol 1994; 251: 245–251
  • DeCoursey P J. “Circadian photoentrainment: parameters of phase delaying”,. J. Biol. Rhythms 1986; 1: 171–186
  • De Kloet E R., Rosenfeld P., van Eekelen J A.M., Sutanto W., Levine S. “Stress, Glucocorticoids and Development”,. Prog. Brain Res 1988; 73: 101–120
  • Dinan T G. “Serotonin and the regulation of hypothalamic-pituitary-adrenal axis function”,. Life Sci 1996; 58: 1683–1694
  • Dugovic C., Maccari S., Weibel L., Turek F W., van Reeth O. “High corticosterone levels in prenatally-stressed rats predict persistent paradoxical sleep alterations”,. J. Neurosci 1999; 19: 8656–8664
  • Dunn A. “Endotoxin-induced activation of cerebral catecholamine and serotonin metabolism: comparison with interleukin-1”,. J. Pharm. Exp. Ther 1992; 261: 964–969
  • Falconer J., Chan E C., Madsen G., Thomson M., Davies J., Smith R. “Secretion of beta-endorphin into the maternal circulation by utero placental tissues in response to hypogly-caemic stress”,. J. Endocr 1988; 118: R5–R8
  • Fride E., Weinstock M. “The effects of prenatal exposure to predictable or unpredictable stress on early development in the rat”,. Dev. Psychobiol 1984; 17: 651–660
  • Fride E., Weinstock M. “Prenatal stress increases anxiety-related behavior and alters cerebral lateralisation of dopaminergic activity”,. Life Sci 1988; 42: 1059–1065
  • Fride E., Dan Y, Feldon J., Halevy G., Weinstock M. “Prenatal stress impairs maternal behavior in a conflict situation and reduces hippocampal benzodiazepine receptors”,. Life Sci 1985; 36: 2103–2109
  • 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
  • Gitau R., Cameron A., Fisk N M., Glover V. “Fetal exposure to maternal cortisol”,. Lancet 1998; 352: 707–708
  • Gold P W., Loriaux D L., Roy A., Kling M A., Calabrese J R., Kellner C H., Nieman L K., Post R M., Pickar D., Galluci W., Avgerinos P., Paul S., Oldfield E H., Cutler G B., Chrousos G. P. “Responses to corticotropin-releasing hormone in the hypercortisolism of depression and Cushing's disease”,. N. Engl. J. Med 1986; 314: 1329–1335
  • Groome L J., Swiber M J., Bentz L S., Holland S B., Atterbury J L. “Maternal anxiety during pregnancy: effect on fetal behavior at 38 to 40 weeks' gestation”,. J. Dev. Behav. Paediatr 1995; 16: 391–396
  • Henry C, Kabbaj M., Simon H., Le Moal M., Maccari S. “Prenatal stress increases the hypofhalamo-pituitary-adrenal axis response in young and adult rats”,. J. Neuroendocrinol 1994; 6: 341–345
  • Holsboer F. “Psychiatric implications of altered limbic-hypothalamic-pituitary-adrenocortical activity”,. Eur. Arch. Psychiat. Neurol. Sci 1989; 238: 302–322
  • Holsboer F., Bardeleben U., Gerken A., Stalla G K., Muller O A. “Blunted corticotropin and normal cortisol response to human corticotropin-releasing-factor in depression”,. N. Engl. J. Med 1984; 311: 1127
  • Hubain P P., Staner L., Dramaix M., Kerkhofs M., Papadimpi-triou G., Mendlewicz J., Linkowski P. “The dexamethasone suppression test and sleep electroencephalogram in nonbipolar major depressed inpatients: a multivariate analysis”,. Biol. Psychiatr 1998; 43: 220–229
  • Huttenen M O. “Persistent alteration of turnover of brain noradrenaline in the offspring of rats subjected to stress during pregnancy”,. Nature 1971; 230: 53–57
  • Ianniruberto A., Tajani E. “Ultrasonographic study of fetal movements”,. Semin. Perinatal 1981; 5: 175–181
  • Janowsky D S., Overstreet D H., Nurnberger J. I. “Is cholinergic sensitivity a genetic marker for the affective disorders?”,. Am. J. Med. Genet 1994; 54: 335–344
  • Joffe J M. Prenatal Determinants of Behavior. Pergamon Press, Oxford 1969
  • Joffe J M. Hormonal Mediation of the Effects of Prenatal Stress on Offspring Behavior Studies in the Development of Behavior and the Nervous System. Academic Press, New York/London 1978; 107–144
  • Kant G J., Pastel R H., Bauman R A. “Effects of chronic stress in sleep”,. Physiol. Behav 1995; 57: 359–365
  • 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
  • Koehl M., Daurnaudery M., Dulluc J., van Reeth O., Le Moal M., Maccari S. “Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corti-costeroid receptors in adult rats of both gender”,. J. Neurobiol 1999; 40: 302–315
  • Konakchieva R., Mitev Y., Almeida O F.X., Patchev V K. “Chronic melatonin treatment and the hypothalamo-pituitary-adrenal axis in the rat: attenuation of the secretory response to stress and effects on hypothalamic neuropeptide content and release”,. Biol. Cell 1997; 89: 587–596
  • Kupfer D J., Reynolds C F. “Sleep and affective disorders”,. Handbook of Affective Disorders, E S. Paykel. Churchill Livingstone, Edinburgh 1992; Vol. 1: 311–323
  • Lecanuet J P., Schaal B., Granier-Deferre C. Sensorialité du fetus. Encyclopedie Medico-Chirurgicale, Paris 1995; 5–002, A-60
  • Lee S., Imaki T., Vale W., Rivier C. “Effect of prenatal exposure to ethanol on the activity of the hypothalamic -pituitary-adrenal axis of the offspring: Importance of the time of exposure to ethanol and possible modulating mechanisms”,. Mol. Cell. Neurosci 1990; 1: 168–177
  • Liu D., Diorio J., Tannenbaum B., Caldji C, Francis D., Freedman A., Sharma S., Pearson D., Plotski P M., Meaney M J. “Maternal care, hippocampal glucocorti-coid receptors, and hypothalamic-pituitary-adrenal responses to stress”,. Science 1997; 277: 1659–1662
  • Maccari S., van Reeth O. Circadian Rhythms and Sleep: Effects of Prenatal Stress in Rodents—An Animal Model for Human Depression Encyclopedia of Stress. Academic Press, NewYork/London 2000; Vol. 1: 1150–1151
  • 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
  • Maccari S., Koehl M., Le Moal M., Dulluc J., Olivares E., van Reeth O. “Prenatal stress induces an advance of both corticosterone and locomotor activity rhythms in adult female rats”,. Soc. Neurosci. Abstr 1997; 522: 11
  • Maccari S., Rettori M C., Koehl M., Weibel L., Dulluc J., van Reeth O. “Corrective effects of tianeptine, melatonin or a melatonin agonist on corticosterone secretion and forced swimming test in prenatally-stressed rats”,. 29th Annual meeting of the Society for Neuroscience, Miami, USA. 1999
  • Marinova C, Persengiev S., Konakchieva R., Ilieva A., Patchev V. “Melatonin effects on glucocorticoid receptors in rat brain and pituitary: significance in adrenocor-tical regulation”,. Int. J. Biochem 1991; 23: 479–481
  • McCormick CM., 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
  • Meier A. “Child psychiatric sequelae of maternal war stress”,. Acta Psychiatr. Scand 1985; 72: 505–511
  • Mikuni M., Kitera K., Saitoh K., Yamazaki C, Okuyama H., Majima T., Ida I., Iijima Y., Takahashi K. “Effects of prenatal stressful stimuli on serotonin content in the hypothalamus and pituitary-adrenal response to conditioned stress in adult offspring”,. Serotonin in the Central Nervous System and Periphery, A. Takada, G. Curzon. Elsevier, Amsterdam 1995; 81–87
  • Miles A., Philbrick D R. “Melatonin and psychiatry”,. Biol Psychiatr 1988; 23: 405–425
  • Mocaër E., Rettori M C., Kamoun A. “Pharmacological antidepressive effects and tianeptine-induced 5HT uptake increase”,. Clin. Neuropharmacol 1988; 11: S32–S42
  • Moreau J L., Scherschicht R., Jenck F., Martin J R. “Chronic mild stress-induced anhedonia model of depression: sleep abnormalities and curative effects of electroshock treatment”,. Behav. Pharmacol 1995; 6: 682–687
  • Moore R Y. “The suprachiasmatic nucleus and the organization of a circadian system”,. Trends Neurosci 1982; 4: 404–407
  • Moore R Y., Eichler V B. “Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat”,. Brain Res 1972; 42: 201–206
  • Muneoka K., Mikuni M., Ogawa T., Kitera K., Kamei K., Takigawa M., Takahashi K. “Prenatal dexametha-sone exposure alters brain monoamine metabolism and adrenocortical response in rat offspring”,. Am. J. Physiol 1997; 273: R1669–R1775
  • Nemeroff C B. “The role of corticotropinyreleasing factor in the pathogenesis of major depression”,. Pharmacopsychiatry 1988; 21: 76–82
  • Neumann I D., Johnstone H A., Hatzinger M., Liebsch G., Shipston M., Russell J A., Landgraf R., Douglas A J. “Attenuated neuroendocrine responses to emotional and physical stressors in pregnant rats involve adenohypophysial changes”,. J. Physiol 1998; 508: 289–300
  • Ohkawa T., Takeshita S., Murase T., Okinaga S., Arai K. “The effect of an acute stress in late pregnancy on hypothalamic catecholamines of the rat fetus”,. Acta Obstet. Gynaecol. Jpn 1991; 43: 783–787
  • Patrick J., Campbell K., Carmichael L., Natale R., Richardson B., Tevaarwerk G. “Effects of synthetic glucocorticoid administration on human fetal breathing movements at 34–35 weeks of gestational age”,. Am. J. Obstet. Gynecol 1981; 139: 324–328
  • Peters D. “Prenatal stress: effects on brain biogenic amine and plasma corticosterone levels”,. Pharmacol. Biochem. Behav 1982; 17: 721–725
  • Peters D A. “Prenatal stress increases the behavioral response to serotonin agonists and alters open field behavior in the rat”,. Pharmacol. Biochem. Behav 1986; 25: 873–877
  • Peters D A. “Both prenatal and postnatal factors contribute to the effects of maternal stress on offspring behavior and central 5-hydroxytryptamine receptors in the rat”,. Pharmacol. Biochem. Behav 1988; 30: 669–673
  • Pittendrigh C. “Circadian systems: general perspective”,. Biological Rhythms Handbook of behavioral neurobiology series, J. Ashoff. Plenum press, New York 1981; Vol. 4: 57–80
  • Poland R E., McCracken J M., Lutchmansingh P., Tondo L. “Relationship between REM sleep latency and nocturnal cortisol concentrations in depressed patients”,. J. Sleep Res 1992; 1: 54–57
  • Poland R E., Lutchmansingh P., McGeoy S., Au D., Que M., Acosta S., McCracken J T. “Prenatal stress prevents the desensitization of the corticosterone response to TFMPP by desmethylimipramine, but not by phenelzine, in adult male offspring”,. Life Sci 1995; 57: 2163–2170
  • Poltyrev T., Weinstock M. “Effect of gestational stress on maternal behavior in response to cage transfer and handling of pups in two strains of rat”,. Stress 1999; 3: 85–95
  • Reppert S M., Schwartz W J. “Maternal coordination of the fetal biological clock in utero”,. Science 1983; 220: 969–971
  • Reppert S M., Schwartz W J. “Maternal endocrine extirpations do not abolish maternal coordination of the fetal circadian clock”,. Endocrinology 1986; 119: 1763–1767
  • Reul J M.H.M., Stec I., Wiegers G J., Labeur M S., Linthorst A C.E., Arzt E., Holsboer F. “Prenatal immune challenge alters the hypothalamic-pituitary-adrenocortical axis in adult rats”,. J. Clin. Invest 1994; 93: 2600–2607
  • Rivier C., Bruhn T., Vale W. “Effect of ethanol on the hypothalamic-pituitary-adrenal axis in the rat: role of cortico-trophin-releasing factor (CRF)”,. J. Pharmacol. Exp. Ther 1984; 229: 127–131
  • Rosenwasser A., Wirz-Justice A. “Circadian Rhythms and Depression: Clinical and Experimental Models”,. Physiology and Pharmacology of Biological Rhythms, P H. Redfern, B. Lemmer. Springer, Berlin 1997; Vol. 125: 457–486
  • Sapolsky R M. “Why stress is bad for your brain”,. Science 1996; 273: 749–750
  • Schell L M. “Environmental noise and human prenatal growth”,. Am. J. Phys. Anthropol 1981; 56: 63–70
  • Schneider M L. “Prenatal stress exposure alters postnatal behavioral expression under conditions of novelty challenge in Rhesus monkey infants”,. Dev. Psychobiol 1992; 25: 529–540
  • Shibata S., Moore R Y. “Development of a fetal circadian rhythm after disruption of the maternal circadian system”,. Dev. Brain. Res 1988; 41: 313–317
  • Stott D N. “Follow-up study from birth of the effects of prenatal stress”,. Dev. Med. Child Neural 1973; 15: 770–787
  • 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
  • Takahashi L K., Turner J G., Kalin N H. “Prenatal stress alters brain catecholaminergic activity and potentiates stress-induced behavior in adult rats”,. Brain Res 1992; 574: 131–137
  • Teixeira J M.A., Fisk N M., Glover V. “Association between maternal anxiety in pregnancy and increased uterine artery resistance index: cohort based study”,. BMJ 1999; 318: 153–157
  • Thompson W R. “Influence of prenatal maternal anxiety on emotionality in young rats”,. Science 1957; 125: 698–699
  • Turek F W., Gwinner E. “Role of hormones in the circadian organization of vertebrates”,. Vertebrate Circadian Systems, J. Ashoff, S. Daan, G. Groos. Springer, Berlin, Heidelberg 1986; 173–182
  • Turek F W., van Reeth O. “Circadian rhythms”,. Handbook of Physiology, M J. Fregly, CM. Blatteis. Oxford University Press, Oxford 1995; Vol. 4: 1329–1359
  • Vallée M., Mayo W., Maccari S., Le Moal M., Simon H. “Long-term effects of prenatal stress and handling on metabolic parameters: relationship to corticosterone secretion response”,. Brain Res 1996; 712: 287–292
  • Vallée M., Mayo W., Delhi 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
  • Vallée M., Maccari S., Dellu F., Simon H., Le Moal M., Mayo W. “Long-term effects of prenatal stress and postnatal handling on age-related glucocorticoid secretion and cognitive performance. A longitudinal study in the rat”,. Eur. J. Neurosci 1999; 11: 2906–2916
  • van Reeth O., Turek F W. “Stimulated activity mediates phase shifts in the hamster circadian clock induced by dark pulses or benzodiazepines”,. Nature 1989; 339: 49–51
  • van Reeth O., Koehl M., Weibel L., Le Moal M., Maccari S. “Effects of prenatal stress on circadian synchronization in adult rats”,. J. Sleep Res 1998; 7: 287
  • Wakshlak A., Weinstock M. “Neonatal handling reverses behavioral abnormalities induced in rats by prenatal stress”,. Physiol. Behav 1990; 48: 289–292
  • Ward I L., Weisz J. “Differential effects of maternal stress on circulating levels of corticosterone, progesterone and testosterone in male and female rat fetus and their mothers”,. Endocrinology 1984; 84: 1145–1635
  • Wehr T A., Wirz-Justice A A. “Circadian rhythm mechanisms in affective illness and in antidepressant drug action”,. Pharmacopsychiatry 1982; 15: 31–39
  • Weinstock M. “Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis?”,. Neurosci. Biobehav. Rev 1997; 21: 1–10
  • Weinstock M., Matline E., Maor G I., Rosen H., McEwen B. “Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary adrenal system in the female rats”,. Brain Res 1992; 595: 195–198
  • Weinstock M., Poltyrev T., Schorer-Apelbaum D., Men D., McCarty R. “Effect of prenatal stress on plasma corticosterone and catecholamines in response to footshock in rats”,. Physiol. Behav 1998; 64: 439–444
  • Whitaker-Azmitia P M., Quartermain D., Shemer A V. “Prenatal treatment with a selective D1 receptor agonist (SKF 38393) alters adult [3H]paroxetine binding and dopamine and serotonin behavioral sensitivity”,. Dev. Brain Res 1990; 57: 181–185
  • Willner P. “Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation”,. Psychopharmacology 1997; 134: 319–329

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