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The Journal of Neuroscience, May 15, 2000, 20(10):3926-3935
Postnatal Handling Increases the Expression of cAMP-Inducible
Transcription Factors in the Rat Hippocampus: The Effects of Thyroid
Hormones and Serotonin
Michael J.
Meaney1,
Josie
Diorio1,
Darlene
Francis1,
Shelley
Weaver1,
Joyce
Yau2,
Karen
Chapman2, and
Jonathan R.
Seckl2
1 Developmental Neuroendocrinology Laboratory, Douglas
Hospital Research Center, Departments of Psychiatry, and Neurology and
Neurosurgery, McGill University, Montreal, Canada, H4H 1R3, and
2 Molecular Endocrinology Laboratory, Department of
Medicine, University of Edinburgh, Edinburgh, Scotland, United Kingdom
EH4 2XU
Postnatal handling increases glucocorticoid receptor expression in
the rat hippocampus, thus altering the regulation of hypothalamic synthesis of corticotropin-releasing hormone and the
hypothalamic-pituitary-adrenal response to stress. The effect on
glucocorticoid receptor gene expression represents one mechanism by
which the early environment can exert a long-term effect on neural
development. The handling effect on hippocampal glucocorticoid receptor
expression is dependent on peripheral thyroid hormone release and the
activation of ascending serotonergic pathways. In primary hippocampal
cell cultures, serotonin (5-HT) increases glucocorticoid receptor
expression, and this effect appears to be mediated by increased cAMP
levels. In the current studies we examined the in vivo
effects of handling on hippocampal cAMP-protein kinase A (PKA)
activity. In 7-d-old rat pups, we found that (1) postnatal handling
increased adenylyl cyclase activity and hippocampal cAMP levels, (2)
the effect of handling on cAMP levels was completely blocked by
treatment with either propylthiouracil (PTU), a thyroid hormone
synthesis inhibitor, or the 5-HT receptor antagonist, ketanserin, and
(3) handling also increased hippocampal PKA activity. We then examined
the effects of handling on cAMP-inducible transcription factors.
Handling rapidly increased levels of the mRNAs for nerve growth
factor-inducible factor A (NGFI-A) (zif268,
krox24) and activator protein-2 (AP-2) as well as for
NGFI-A and AP-2 immunoreactivity throughout the hippocampus. Finally,
we found that the effects of handling on NGFI-A and AP-2 expression
were significantly reduced by concurrent treatment with either PTU or
ketanserin, effects that paralleled those on cAMP formation. NGFI-A and
AP-2 have been implicated in the regulation of glucocorticoid receptor
expression during development. Thus, these findings suggest that
postnatal handling might alter glucocorticoid receptor gene expression
via cAMP-PKA pathways involving the activation of NGFI-A and AP-2.
Key words:
glucocorticoid receptor; neural development; cAMP; thyroid hormones; serotonergic pathways; rat
Copyright © 2000 Society for Neuroscience 0270-6474/00/20103926-10$05.00/0
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