Estrogen modulates stimulation of inositol phospholipid hydrolysis by norepinephrine in rat brain slices

doi:10.1016/0006-8993(91)90860-X

Brain Research

Volume 555, Issue 1, 26 July 1991, Pages 65-69

https://doi.org/10.1016/0006-8993(91)90860-X Get rights and content

Abstract

The influence of estrogen on stimulation of inositol phospholipid hydrolysis by norepinephrine and carbamylcholine has been studied by measuring the accumulation of [³H]inositolmonophosphate ([³H]InsP) in cortical, hippocampal and striatal slices from ovariectomized rats. Repeated (but not a single) subcutaneous injections of estradiol benzoate (EB) (2 μg/animal once every 2 days for 10 days) markedly reduced stimulation of inositol phospholipid hydrolysis by norepinephrine in hippocampus and corpus striatum. Conversely, the efficacy of norepinephrine was increased in cortical slices. Estrogen treatment did not affect basal or carbamylcholine-stimulated [³H]InsP formation. In vitro addition of 17β-estradiol (1–100 nM) failed to modify norepinephrine- or carbamylcholine-induced [³H]InsP production in all regions examined. An increased density ofα₁-adrenergic binding sites in cortical membranes paralleled the enhanced responsiveness of inositol phospholipid hydrolysis to norepinephrine induced by EB treatment in this area, whereas no significant changes in [³H]prazosin binding were found in membranes from hippocampus and corpus striatum. These results indicate that estrogen may affect inositol phospholipid hydrolysis in discrete brain areas, suggesting a complex role for estradiol in modulating noradrenergic receptor activity in the central nervous system.

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Estrogens act in diverse brain regions to regulate reproductive and nonreproductive behaviors and neuronal functions, including mood, cognition, pain, seizures, sensorimotor integration, energy homeostasis, and neural degeneration due to aging, ischemia, and other insults. This chapter reviews evidence that estrogens act at multiple levels in many brain regions to modify synaptic neurotransmission. Identified targets of estrogen action include classical neurotransmitters and diverse peptides that function as neuromodulators. Estrogens act both presynaptically, regulating transmitter availability and/or release, and postsynaptically, governing cellular responses to released transmitter. Hormone-dependent alterations in neural responses to transmitters involve regulation of transmitter receptor expression and the efficacy of transmembrane signal transduction. Estrogens also determine which intracellular signal transduction pathways are activated when neurotransmitters bind their receptors. Emerging evidence suggests that estrogens can activate downstream molecules associated with growth factors and modify the crosstalk between growth factor and neurotransmitter receptor signaling pathways. Therefore, we also summarize findings indicating that physiologically relevant cross talk occurs among estrogen receptor, neurotransmitter receptor, and growth factor receptor signal transduction pathways. The data show that estrogens act throughout the brain to modulate neuronal excitability, synaptic efficacy, and neurogenesis, suggesting that these are fundamental mechanisms of steroid hormone action in the brain.
α<inf>1</inf>-Noradrenegic receptor antagonism disrupts female songbird responses to male song
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Female songbirds respond behaviorally to differences in male song structure. Past data suggest a complex role for norepinephrine in female responses to song. Here, we examined the effects of central infusions of the α₁-noradrenergic receptor antagonist prazosin on female European starling (Sturnus vulgaris) responses to nest boxes broadcasting male song. Prazosin disrupted female preferential responses to male starling song over the less biologically relevant purple martin (Progne subis) song. Prazosin decreased female responses to male starling song in a linear dose–response fashion; whereas, it affected responses to purple martin song in a U-shaped dose–response fashion. Results suggest that the role of norepinephrine in female responses to male song differs depending upon drug dose and the biological relevance of the song stimulus.
Estrogen regulation of neurotransmitter and growth factor signaling in the brain
2009, Hormones, Brain and Behavior Online
Estrogens act in diverse brain regions to regulate reproductive and nonreproductive behaviors and neuronal functions, including mood, cognition, pain, seizures, sensorimotor integration, energy homeostasis, and neural degeneration due to aging, ischemia, and other insults. This chapter reviews evidence that estrogens act at multiple levels in many brain regions to modify synaptic neurotransmission. Identified targets of estrogen action include classical neurotransmitters and diverse peptides that function as neuromodulators. Estrogens act both presynaptically, regulating transmitter availability and/or release, and postsynaptically, governing cellular responses to released transmitter. Hormone-dependent alterations in neural responses to transmitters involve regulation of transmitter receptor expression and the efficacy of transmembrane signal transduction. Estrogens also determine which intracellular signal transduction pathways are activated when neurotransmitters bind their receptors. Emerging evidence suggests that estrogens can activate downstream molecules associated with growth factors and modify the crosstalk between growth factor and neurotransmitter receptor signaling pathways. Therefore, we also summarize findings indicating that physiologically relevant cross talk occurs among estrogen receptor, neurotransmitter receptor, and growth factor receptor signal transduction pathways. The data show that estrogens act throughout the brain to modulate neuronal excitability, synaptic efficacy, and neurogenesis, suggesting that these are fundamental mechanisms of steroid hormone action in the brain.
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2006, Knobil and Neill's Physiology of Reproduction
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Effects of chronic restraint stress and estradiol on open field activity, spatial memory, and monoaminergic neurotransmitters in ovariectomized rats
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Twenty-one days of chronic restraint stress impairs male rat performance on the radial arm maze [Luine et al. (1994) Brain Res. 639, 167–170], but enhances female rat performance [Bowman et al. (2001) Brain Res. 904, 279–289]. To assess possible ovarian hormone mechanisms underlying this sexually dimorphic response to stress, we examined chronic stress effects in ovariectomized rats. Ovariectomized rats received Silastic capsule implants containing cholesterol or estradiol and were assigned to a daily restraint stress (21 days, 6 h/day) or non-stress group. Following the stress period, subjects were tested for open field activity and radial arm maze performance. Stress and estradiol treatment affected open field activity. All stressed animals, with or without estradiol treatment, made fewer total outer sector crossings. In contrast, estradiol-treated animals, with or without stress, made more inner sector visits, an indication that estradiol decreased anxious behavior on the open field across time. As measured by the total number of visits required to complete the task, stress did not affect radial arm maze performance in ovariectomized rats, but estradiol-treated animals, with or without stress, performed better than non-treated animals on the radial arm maze. Stressed subjects receiving estradiol showed the best radial arm maze performance. Following killing, tissue samples were obtained from various brain regions known to contribute to learning and memory, and monoamine and metabolite levels were measured. Several changes were observed in response to both stress and estradiol. Most noteworthy, stress treatment decreased homovanillic acid levels in the prefrontal cortex, an effect not previously observed in stressed intact females. Estradiol treatment increased norepinephrine levels in CA3 region of the hippocampus, mitigating stress-dependent changes. Both stress and estradiol decreased dentate gyrus levels of 5-hydroxyindole acetic acid.
In summary, the current study provides novel information showing that estradiol alters behavioral and neurochemical responses to stress in ovariectomized rats. Estradiol treatment decreased anxious behavior on the open field and stressed animals receiving estradiol had enhanced radial arm maze performance. In relation to interactions between stress and estradiol on cognition and anxiety, changes in the prefrontal cortex dopaminergic system, dentate gyrus serotonergic system, and norepinephrine levels in the CA3 region appear important. Results show that estradiol may moderate stress effects on cognition and anxiety through both organizational and activation effects.

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Abstract

References (25)

Dopamine-stimulated adenylate cyclase in hypothalamus: influence of estrous cycle in female and castration in male rats

Brain Research

c-fos induction by estrogen in specific rat brain areas

Eur. J. Pharmacol., Mol. Pharmacol. Sect.

Norepinephrine-stimulated cyclic AMP accumulation in rat hypothalamic slices: effects of estrous cycle and ovarian steroids

Brain Research

Gonadal steroid modulation of neurotransmitters stimulated cAMP accumulation in the hippocampus of the rat

Brain Research

Progesterone and estrogens in rat brain: modulation of γ-aminobutyric acid receptor activity

Eur. J. Pharmacol.

Functional receptor for neurotransmitters on astroglial cells

Neuroscience

Estrogen administration increases neuronal responses to excitatory amino acids as a long-term effect

Brain Research

Sex steroid on extrahypothalamic CNS. I. Estrogen augments neuronal responsiveness to iontophoretically applied glutamate in the cerebellum

Brain Research

Effect of estradiol on alpha- and beta-adrenoreceptor density in medial basal hypothalamus, cerebral cortex and pineal gland of ovariectomized rats

Neurosci. Lett.

Decreased β-adrenergic responses in female rat brain are eliminated by ovariectomy: correlation of [³H]dihydroalprenolol binding and catecholamine-stimulated cyclic AMP levels

Brain Research

Estrogens, progesterone, and the extrapyramidal system

Inositol trisphosphate and diacylglycerol: two interacting second messengers

Annu. Rev. Biochem.

Cited by (37)

Estrogen Regulation of Neurotransmitter and Growth Factor Signaling in the Brain

α<inf>1</inf>-Noradrenegic receptor antagonism disrupts female songbird responses to male song

Estrogen regulation of neurotransmitter and growth factor signaling in the brain

Hormonal, neural, and genomic mechanisms for female reproductive behaviors, motivation, and arousal

Hormonal, Neural, and Genomic Mechanisms for Female Reproductive Behaviors, Motivation, and Arousal

Effects of chronic restraint stress and estradiol on open field activity, spatial memory, and monoaminergic neurotransmitters in ovariectomized rats