Psychoneuroendocrinology
Volume 31, Issue 6 , Pages 769-780 , July 2006

Prenatal stress alters Fos protein expression in hippocampus and locus coeruleus stress-related brain structures

  • Odile Viltart

      Affiliations

    • Laboratory of Perinatal Stress, JE2365, University of Lille 1, 59655 Villeneuve d'Ascq, France
    • O. Viltart and J. Mairesse contribute equally to the work presented here.
  • ,
  • Jérôme Mairesse

      Affiliations

    • Laboratory of Perinatal Stress, JE2365, University of Lille 1, 59655 Villeneuve d'Ascq, France
    • O. Viltart and J. Mairesse contribute equally to the work presented here.
  • ,
  • Muriel Darnaudéry

      Affiliations

    • Laboratory of Perinatal Stress, JE2365, University of Lille 1, 59655 Villeneuve d'Ascq, France
  • ,
  • Hélène Louvart

      Affiliations

    • Laboratory of Perinatal Stress, JE2365, University of Lille 1, 59655 Villeneuve d'Ascq, France
  • ,
  • Christel Vanbesien-Mailliot

      Affiliations

    • Laboratory of Perinatal Stress, JE2365, University of Lille 1, 59655 Villeneuve d'Ascq, France
  • ,
  • Assia Catalani

      Affiliations

    • Laboratory of Pharmacology, Dip Erspamer, University of Rome1 ‘La Sapienza’, 00185 Rome, Italy
  • ,
  • Stefania Maccari

      Affiliations

    • Laboratory of Perinatal Stress, JE2365, University of Lille 1, 59655 Villeneuve d'Ascq, France
    • Department of Experimental Medicine and Pathology, University Rome1 ‘La Sapienza’, Rome, Italy
    • Corresponding Author InformationCorresponding author. Address: Laboratory Neurophysiology/Perinatal Stress, Departement of Biology, University of Lille 1, Cite Scientifique, Batiment SN4.1, 59655 Villeneuve d'Ascq, France. Fax: +33 3 20 43 46 02.

Received 30 November 2005 ,Revised 18 February 2006 ,Accepted 19 February 2006.

References 

  1. Barbazanges A, Vallée M, Mayo W, Day J, Simon H, Le Moal M, et al. Early and later adoptions have different long-term effects on male rat offspring. J. Neurosci. 1996;16:7783–7790
  2. Boudaba C, Szabo K, Tasker JG. Physiological mapping of local inhibitory inputs to the hypothalamic paraventricular nucleus. J. Neurosci. 1996;16:7151–7160
  3. Bowers G, Cullinan WE, Herman JP. Region-specific regulation of glutamic acid decarboxylase (GAD) mRNA expression in central stress circuits. J. Neurosci. 1998;18:5938–5947
  4. Chapman RH, Stern JM. 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;12:255–267
  5. Chapillon P, Patin V, Roy V, Vincent A, Caston J. Effects of pre- and postnatal stimulation on developmental, emotional, and cognitive aspects in rodents: a review. Dev. Psychobiol. 2002;41:373–387
  6. Cullinan WE, Herman JP, Watson SJ. Ventral subicular interaction with the hypothalamic paraventricular nucleus: evidence for a relay in the bed nucleus of stria terminalis. J. Comp. Neurol. 1993;332:1–20
  7. Daftary SS, Boudaba C, Tasker JG. Noradrenergic regulation of parvocellular neurons in the rat hypothalamic paraventricular nucleus. Neuroscience. 2000;96:743–751
  8. Day HE, Campeau S, Watson SJ. Expression of (1b) adrenoreceptor mRNA in corticotropin-releasing hormone-containing cells in the rat hypothalamus on its regulation by corticosterone. J. Neurosci. 1999;19:10098–10106
  9. Diamond MI, Miner JN, Yoshinaga SK, Yamamoto KR. Transcription factor interactions: selectors of positive or negative regulation from a single DNA element. Science. 1990;249:1266–1272
  10. Dugovic C, Maccari S, Weibel L, Turek FW, Van Reeth O. Corticosterone levels in prenatally stressed rats predict persistent paradoxical sleep alterations. J. Neurosci. 1999;19:8564–8656
  11. Han SK, Chong W, Li LH, Lee IS, Murase K, Ryu PD. Noradrenaline excites and inhibits GABAergic transmission in parvocellular neurons of rat hypothalamic paraventricular nucleus. J. Neurophysiol. 2002;87:2287–2296
  12. Herdegen T, Leah JD. Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res. Rev. 1998;28:370–490
  13. Herman JP, Cullinan WE. Neurocircuitry of stress: central control of the hypothalamopituitary–adrenocortical axis. Trends Neurosci. 1997;20:78–84
  14. Herman JP, Cullinan WE, Ziegler DR, Tasker JG. Role of the paraventricular nucleus microenvironment in stress integration. Eur. J. Neurosci. 2002;16:381–383
  15. Herman JP, Mueller NK, Figueiredo H. Role of GABA and glutamate circuitry in hypothalamo-pituitary–adrenocortical stress integration. Ann. NY Acad. Sci. 2004;1018:35–45
  16. Kabbaj M, Piazza PV, Simon H, Le Moal M, Maccari S. Opposite effects on hippocampal corticosteroid receptors induced by stimulation of beta and alpha 1 noradrenergic receptors. Neuroscience. 1995;66:539–545
  17. 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
  18. Krukoff TL. C-fos expression as a marker of functional activity in the brain. In:  Bouton AA,  Baker GB,  Bateson AN editor. Cell Neurobiology Techniques, Neuromethods. vol. 33:Clifton, UK: Humana Press; 1999;p. 213–229
  19. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–685
  20. Lai M, McCormick JA, Chapman KE, Kelly PA, Seckl JR, Yau JL. Regulation of corticosteroid receptors by monoamine neurotransmitters and antidepressant drugs in primary hippocampal culture. Neuroscience. 2003;118:975–984
  21. Landgraf R, Wigger A, Hoelsboer F, Neuman D. Hyper reactive hypothalamopituitary-adrenocortical axis in rats bred for high anxiety-related behaviour. J. Neuroendocrinol. 1999;11:405–407
  22. Maccari S, Mormède P, Piazza PV, Simon H, Angelucci L, Le Moal M. Hippocampal type I and type II corticosteroid receptors are modulated by central noradrenergic systems. Psychoneuroendocrinology. 1992;17:103–112
  23. Maccari S, Piazza PV, 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
  24. Maccari S, Darnaudery M, Morley-Fletcher S, Zuena AR, Cinque C, Van Reeth O. Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci. Biobehav. Rev. 2003;27:119–127
  25. McCormick CM, Smythe JW, Sharma S, Meaney MJ. Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoïds receptor density in adult rats. Dev. Brain Res. 1995;84:55–61
  26. McEwen BS, Wingfield JC. The concept of allostasis in biology and biomedicine. Horm. Behav. 2003;43:2–15
  27. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM. Identification and characterization of the vesicular GABA transporter. Nature. 1997;389:870–876
  28. Morley-Fletcher S, Darnaudery M, Koehl M, Casolini P, Van Reeth O, Maccari S. Prenatal stress in rats predicts immobility behaviour in the forced swim test. Effects of a chronic treatment with tianeptine. Brain Res. 2003;989:246–251
  29. 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
  30. Muneoka K, Mikuni M, Ogawa T, Kitera K, Kamei K, Takigawa M, et al. Prenatal dexamethasone exposure alters brain monoamine metabolism and adrenocortical response in rat offspring. Am. J. Physiol. 1997;273:1669–1675
  31. Pace TW, Gaylord R, Topczewski F, Girotti M, Rubin B, Spencer RL. Immediate-early gene induction in hippocampus and cortex as a result of novel experience is not directly related to the stressfulness of that experience. Eur. J. Neurosci. 2005;22:1679–1690
  32. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. Compact 3rd ed.. San Diego, CA: Academic Press; 1997;
  33. Peters DA. Prenatal stress: effect on development of rat brain serotonergic neurons. Pharmacol. Biochem. Behav. 1986;24:1377–1382
  34. Plotsky PM. Facilitation of immunoreactive corticotropin-releasing factor secretion into the hypophyseal-portal circulation after activation of catechoaminergic pathways or central norepinepherine injection. Endocrinology. 1987;121:924–930
  35. Poland RE, Lutchmansingh P, McGeoy S, Au D, Que M, Acosta S, et al. 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
  36. Saphier D. Catecholaminergic projections to tuberoinfundibular neurones of the paraventricular nucleus: I. Effects of stimulation of A1, A2, A6 and C2 cell groups. Brain Res. Bull. 1989;23:389–395
  37. Sapolsky RM, Krey LC, McEwen BS. Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc. Natl Acad. Sci. USA. 1984;81:6174–6177
  38. Shu SY, Ju G, Fan LZ. The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci. Lett. 1988;85:169–171
  39. Takahashi LK, Kalin NH. Early developmental and temporal characteristics of stress induced secretion of pituitary-adrenal hormones in prenatally stressed rat pups. Brain Res. 1991;558:75–78
  40. Takahashi LK, Turner JG, Kalin NH. Prenatal stress alters brain catecholaminergic activity and potentiates stress-induced behaviour in adult rats. Brain Res. 1992;574:131–138
  41. Takamori S, Rhee JS, Rosenmund C, Jahn R. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature. 2000;40:189–194
  42. Unlap T, Jope RS. Dexamethasone attenuates kainate-induced AP-1 activation in rat brain. Mol. Brain Res. 1994;24:275–282
  43. Vallée 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
  44. Vallée M, Maccari S, Dellu F, Le Moal M, Simon H, 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
  45. Viltart O, Mullier O, Bernet F, Poulain P, Ba-M'Hamed S, Sequeira H. Motor cortical control of cardiovascular bulbar neurones projecting to spinal autonomic areas. J. Neurosci. Res. 2003;73:122–135
  46. Weinstock M. The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav. Immun. 2005;19:296–308
  47. Weinstock M, Matlina E, Maor GI, Rosen H, McEwen BS. Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary adrenal system in the female rat. Brain Res. 1992;595:195–200
  48. Yang-Yen HF, Chambard JC, Sun YL, Smeal T, Schmidt TJ, Drouin J, et al. Transcriptional interference between c-Jun and the glucocorticoid receptor: mutual inhibition of DNA binding due to direct protein–protein interaction. Cell. 1990;62:1205–1215
  49. Ziegler DR, Cass WA, Herman JP. Excitatory influence of the locus coeruleus in hypothalamic-pituitary–adrenocortical axis responses to stress. J. Neuroendocrinol. 1999;11:361–369

PII: S0306-4530(06)00034-5

doi: 10.1016/j.psyneuen.2006.02.007

Psychoneuroendocrinology
Volume 31, Issue 6 , Pages 769-780 , July 2006