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

Psychoneuroendocrinology

Volumn 31, Issue 6, 2006, Pages 769-780

  Viltart, Odile ^a   Mairesse, Jérôme ^a   Darnaudéry, Muriel ^a   Louvart, Hélène ^a   Vanbesien Mailliot, Christel ^a   Catalani, Assia ^b   Maccari, Stefania ^a,b  

^a UNIV LILLE   (France)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

HPA axis; Locus coeruleus; Noradrenaline Hippocampus; Paraventricular nucleus; Restraint maternal stress

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CORTICOSTEROID; PROTEIN FOS;

ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; BRAIN REGION; CONTROLLED STUDY; CORTICOSTEROID BLOOD LEVEL; FEMALE; HIPPOCAMPUS; HORMONE RESPONSE; HUMAN; IMMUNOREACTIVITY; LOCUS CERULEUS; MAGNITUDE ESTIMATION METHOD; MAZE TEST; NONHUMAN; PRENATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STRESS; SYNAPTIC POTENTIAL;

ANIMALS; CORTICOSTERONE; FEMALE; HIPPOCAMPUS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LOCUS COERULEUS; MALE; NEURONS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; STRESS, PSYCHOLOGICAL; TISSUE DISTRIBUTION; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 33646673606     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2006.02.007     Document Type: Article

References (49)

1. Barbazanges A., Vallée M., Mayo W., Day J., Simon H., Le Moal M., and Maccari S. Early and later adoptions have different long-term effects on male rat offspring. J. Neurosci. 16 (1996) 7783-7790
2. Boudaba C., Szabo K., and Tasker J.G. Physiological mapping of local inhibitory inputs to the hypothalamic paraventricular nucleus. J. Neurosci. 16 (1996) 7151-7160
3. Bowers G., Cullinan W.E., and Herman J.P. Region-specific regulation of glutamic acid decarboxylase (GAD) mRNA expression in central stress circuits. J. Neurosci. 18 (1998) 5938-5947
4. Chapman R.H., and Stern J.M. 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. 12 (1979) 255-267
5. Chapillon P., Patin V., Roy V., Vincent A., and Caston J. Effects of pre- and postnatal stimulation on developmental, emotional, and cognitive aspects in rodents: a review. Dev. Psychobiol. 41 (2002) 373-387
6. Cullinan W.E., Herman J.P., and Watson S.J. Ventral subicular interaction with the hypothalamic paraventricular nucleus: evidence for a relay in the bed nucleus of stria terminalis. J. Comp. Neurol. 332 (1993) 1-20
7. Daftary S.S., Boudaba C., and Tasker J.G. Noradrenergic regulation of parvocellular neurons in the rat hypothalamic paraventricular nucleus. Neuroscience 96 (2000) 743-751
8. Day H.E., Campeau S., and Watson Jr. S.J. Expression of (1b) adrenoreceptor mRNA in corticotropin-releasing hormone-containing cells in the rat hypothalamus on its regulation by corticosterone. J. Neurosci. 19 (1999) 10098-10106
9. Diamond M.I., Miner J.N., Yoshinaga S.K., and Yamamoto K.R. Transcription factor interactions: selectors of positive or negative regulation from a single DNA element. Science 249 (1990) 1266-1272
10. Dugovic C., Maccari S., Weibel L., Turek F.W., and Van Reeth O. Corticosterone levels in prenatally stressed rats predict persistent paradoxical sleep alterations. J. Neurosci. 19 (1999) 8564-8656
11. Han S.K., Chong W., Li L.H., Lee I.S., Murase K., and Ryu P.D. Noradrenaline excites and inhibits GABAergic transmission in parvocellular neurons of rat hypothalamic paraventricular nucleus. J. Neurophysiol. 87 (2002) 2287-2296
12. Herdegen T., and Leah J.D. 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. 28 (1998) 370-490
13. Herman J.P., and Cullinan W.E. Neurocircuitry of stress: central control of the hypothalamopituitary-adrenocortical axis. Trends Neurosci. 20 (1997) 78-84
14. Herman J.P., Cullinan W.E., Ziegler D.R., and Tasker J.G. Role of the paraventricular nucleus microenvironment in stress integration. Eur. J. Neurosci. 16 (2002) 381-383
15. Herman J.P., Mueller N.K., and Figueiredo H. Role of GABA and glutamate circuitry in hypothalamo-pituitary-adrenocortical stress integration. Ann. NY Acad. Sci. 1018 (2004) 35-45
16. Kabbaj M., Piazza P.V., Simon H., Le Moal M., and Maccari S. Opposite effects on hippocampal corticosteroid receptors induced by stimulation of beta and alpha 1 noradrenergic receptors. Neuroscience 66 (1995) 539-545
17. Koehl M., Darnaudery M., Dulluc J., Van Reeth O., Le Moal M., and Maccari S. Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both gender. J. Neurobiol. 40 (1999) 302-315
18. Krukoff T.L. C-fos expression as a marker of functional activity in the brain. In: Bouton A.A., Baker G.B., and Bateson A.N. (Eds). Cell Neurobiology Techniques, Neuromethods vol. 33 (1999), Humana Press, Clifton, UK 213-229
19. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
20. Lai M., McCormick J.A., Chapman K.E., Kelly P.A., Seckl J.R., and Yau J.L. Regulation of corticosteroid receptors by monoamine neurotransmitters and antidepressant drugs in primary hippocampal culture. Neuroscience 118 (2003) 975-984
21. Landgraf R., Wigger A., Hoelsboer F., and Neuman D. Hyper reactive hypothalamopituitary-adrenocortical axis in rats bred for high anxiety-related behaviour. J. Neuroendocrinol. 11 (1999) 405-407
22. Maccari S., Mormède P., Piazza P.V., Simon H., Angelucci L., and Le Moal M. Hippocampal type I and type II corticosteroid receptors are modulated by central noradrenergic systems. Psychoneuroendocrinology 17 (1992) 103-112
23. Maccari S., Piazza P.V., Kabbaj M., Barbazanges A., Simon H., and Le Moal M. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J. Neurosci. 15 (1995) 110-116
24. Maccari S., Darnaudery M., Morley-Fletcher S., Zuena A.R., Cinque C., and Van Reeth O. Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci. Biobehav. Rev. 27 (2003) 119-127
25. McCormick C.M., Smythe J.W., Sharma S., and Meaney M.J. Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoïds receptor density in adult rats. Dev. Brain Res. 84 (1995) 55-61
26. McEwen B.S., and Wingfield J.C. The concept of allostasis in biology and biomedicine. Horm. Behav. 43 (2003) 2-15
27. McIntire S.L., Reimer R.J., Schuske K., Edwards R.H., and Jorgensen E.M. Identification and characterization of the vesicular GABA transporter. Nature 389 (1997) 870-876
28. Morley-Fletcher S., Darnaudery M., Koehl M., Casolini P., Van Reeth O., and Maccari S. Prenatal stress in rats predicts immobility behaviour in the forced swim test. Effects of a chronic treatment with tianeptine. Brain Res. 989 (2003) 246-251
29. Morley-Fletcher S., Darnaudery M., Mocaer E., Froger N., Lanfumey L., Laviola G., Casolini P., Zuena A.R., Marzano L., Hamon M., and Maccari S. Chronic treatment with imipramine reverses immobility behaviour, hippocampal corticosteroid receptors and cortical 5-HT(1A) receptor mRNA in prenatally stressed rats. Neuropharmacology 47 (2004) 841-847
30. Muneoka K., Mikuni M., Ogawa T., Kitera K., Kamei K., Takigawa M., and Takahashi K. Prenatal dexamethasone exposure alters brain monoamine metabolism and adrenocortical response in rat offspring. Am. J. Physiol. 273 (1997) 1669-1675
31. Pace T.W., Gaylord R., Topczewski F., Girotti M., Rubin B., and Spencer R.L. 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. 22 (2005) 1679-1690
32. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates. Compact 3rd ed. (1997), Academic Press, San Diego, CA
33. Peters D.A. Prenatal stress: effect on development of rat brain serotonergic neurons. Pharmacol. Biochem. Behav. 24 (1986) 1377-1382
34. Plotsky P.M. Facilitation of immunoreactive corticotropin-releasing factor secretion into the hypophyseal-portal circulation after activation of catechoaminergic pathways or central norepinepherine injection. Endocrinology 121 (1987) 924-930
35. Poland R.E., Lutchmansingh P., McGeoy S., Au D., Que M., Acosta S., and 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. 57 (1995) 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. 23 (1989) 389-395
37. Sapolsky R.M., Krey L.C., and McEwen B.S. Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc. Natl Acad. Sci. USA 81 (1984) 6174-6177
38. Shu S.Y., Ju G., and Fan L.Z. The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci. Lett. 85 (1988) 169-171
39. Takahashi L.K., and Kalin N.H. Early developmental and temporal characteristics of stress induced secretion of pituitary-adrenal hormones in prenatally stressed rat pups. Brain Res. 558 (1991) 75-78
40. Takahashi L.K., Turner J.G., and Kalin N.H. Prenatal stress alters brain catecholaminergic activity and potentiates stress-induced behaviour in adult rats. Brain Res. 574 (1992) 131-138
41. Takamori S., Rhee J.S., Rosenmund C., and Jahn R. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 40 (2000) 189-194
42. Unlap T., and Jope R.S. Dexamethasone attenuates kainate-induced AP-1 activation in rat brain. Mol. Brain Res. 24 (1994) 275-282
43. Vallée M., Mayo W., Dellu F., Le Moal M., Simon H., and Maccari S. Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J. Neurosci. 17 (1997) 2626-2636
44. Vallée M., Maccari S., Dellu F., Le Moal M., Simon H., and 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. 11 (1999) 2906-2916
45. Viltart O., Mullier O., Bernet F., Poulain P., Ba-M'Hamed S., and Sequeira H. Motor cortical control of cardiovascular bulbar neurones projecting to spinal autonomic areas. J. Neurosci. Res. 73 (2003) 122-135
46. Weinstock M. The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav. Immun. 19 (2005) 296-308
47. Weinstock M., Matlina E., Maor G.I., Rosen H., and McEwen B.S. Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary adrenal system in the female rat. Brain Res. 595 (1992) 195-200
48. Yang-Yen H.F., Chambard J.C., Sun Y.L., Smeal T., Schmidt T.J., Drouin J., and Karin M. Transcriptional interference between c-Jun and the glucocorticoid receptor: mutual inhibition of DNA binding due to direct protein-protein interaction. Cell 62 (1990) 1205-1215
49. Ziegler D.R., Cass W.A., and Herman J.P. Excitatory influence of the locus coeruleus in hypothalamic-pituitary-adrenocortical axis responses to stress. J. Neuroendocrinol. 11 (1999) 361-369