Estradiol induces oxytocin binding sites in rat hypothalamic ventromedial nucleus

Kloet, E. Ronald de; Voorhuis, Th.A.M.; Elands, Jack

doi:10.1016/0014-2999(85)90679-x

Cited by 124 publications

(55 citation statements)

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“…In any case, the facilitation is estrogen dependent. Moreover, ovarian steroids can stimulate the synthesis of OT mRNA in the brain [7][8][9], These findings are consistent with demonstrations showing that estradiol affects the level of OT peptide in the brain [3,[10][11][12], Estrogen also increases OT re ceptor binding in certain brain regions such as the ventrolateral portion of the ventromedial nucleus (vIVMN) of the hypothala mus [13][14][15][16][17][18], the central nucleus of the amygdala [14,19], the bed nucleus of the stria terminalis [20] and the anterior olfactoiy , the expansion brought on by progesterone would bring OT receptors into con tact with a source of endogenous OT. Experimental application of OT to this expanded OT binding region, but not a region anterior to it, facilitated lordosis in rats primed with estrogen and progesterone, but not in rats given estrogen alone [5,6], Thus, it is reasonable to hypothesize that estrogen causes an increase in OT receptors leading to a potentiation of the neu ronal responsiveness to OT, that in turn results in the facilitation of lordosis by OT.…”

supporting

confidence: 77%

“…Secondly, estrogen had no effect on neuronal responsiveness to AVP (table 2). In this respect, it is interesting to note that estrogen was found to have no effect on AVP bind ing in the hypothalamus [13,46]. These specificities indicate that estrogen did not potentiate neuronal responses to OT by simply increasing the general excitability of the neuron.…”

Section: Discussionmentioning

confidence: 98%

“…Both show that estrogen has a facilitatory effect: OT binding was 4-fold increased [16], and neuronal electrical re sponsiveness to OT was strongly potentiated (present study). Similarly, neither type of study found AVP binding [ 13,46] or neuronal responsiveness to AVP (table 2) affected by estrogen. Finally, the neurons affected by estrogen either for OT binding or response to OT are likely to be from the same population because they all are located in the vlVMN.…”

Section: Discussionmentioning

confidence: 99%

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Electrophysiological Actions of Oxytocin on Hypothalamic Neurons in vitro: Neuropharmacological Characterization and Effects of Ovarian Steroids

Kow¹,

Johnson²,

Ogawa³

et al. 1991

Neuroendocrinology

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Oxytocin (OT) neurotransmission in the brain has a facilitatory effect on sexual receptivity in rats. This effect of OT is dependent on priming by ovarian steroids, estrogen and progesterone. These steroids modulate OT binding in specific brain nuclei, including the ventrolateral portion of the ventromedial hypothalamic nucleus (vlVMN). In the present study, single-unit activity was recorded from the vlVMN in hypothalamic slices to characterize the electrophysiological actions of OT. To examine the effects of ovarian steroids on OT actions, we used brain slices prepared from ovariectomized rats either treated with estrogen or not, and some slices were treated with progesterone in vitro. OT had little modulatory action on neuronal responses to other agents, but affected the activity of large numbers of vlVMN units. Of those neurons affected, 94% responded with excitation. This predominant stimulatory action of OT is consistent with its lordosis-facilitating effect, because increases in the activity of VMN neurons are generally associated with the facilitation of lordosis. Pharmacological analyses with selective OT agonists and antagonists as well as structurally related peptides showed that the excitatory action of OT is mediated by OT receptors. Estradiol modulated several aspects of OT transmission. First, it increased neuronal responsiveness to OT, especially at the lowest concentration used (0.2 nM). In addition, it caused neuronal responses to OT to correlate significantly with responses to acetylcholine and norepinephrine, which also can act on the ventromedial hypothalamus to facilitate lordosis. Finally, estradiol enhanced the excitability of laterally projecting neurons, which have been implicated in lordosis. In estrogen-pretreated slices, addition of progesterone in vitro caused little further effect on responses of individual neurons to exogenous OT. Altogether, the present electrophysiological findings are consistent with the hypothesis that estrogen potentiates OT action by increasing functional OT receptors preferentially in lordosis-relevant neurons, thereby enabling OT to efficiently facilitate female reproductive behavior.

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supporting

confidence: 77%

Section: Discussionmentioning

confidence: 98%

Section: Discussionmentioning

confidence: 99%

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Electrophysiological Actions of Oxytocin on Hypothalamic Neurons in vitro: Neuropharmacological Characterization and Effects of Ovarian Steroids

Kow¹,

Johnson²,

Ogawa³

et al. 1991

Neuroendocrinology

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“…Regulation of OTR by estrogens in VMN has been shown in females as well as males (16,18,(20)(21)(22)(23)(24)(25). A four-gene micronet theory featuring ER␣, ER␤, oxytocin, and OTR and has been proposed to explain how neurons in hypothalamus and amygdala cooperate to facilitate social behaviors in female rodents (26,27).…”

mentioning

confidence: 99%

Sex and estrogenic effects on coexpression of mRNAs in single ventromedial hypothalamic neurons

Devidze

Mong

Jasnow

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

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(102, 14446-14451; first published September 26, 2005; 10.1073͞pnas.0507144102), the authors note that ''%'' was added after several numbers, due to a printer's error. On page 14449, right column, the second sentence under Estrogen Treatment Increases Number of ER␣, ER␤, OTR, and PKCs in Female Rats, ''In estrogen-treated animals, these numbers were higher than in the oil group, ER␣ (66% vs. 20%), ER␤ (39% vs. 14%), OTR (56% vs. 15%), PKC␦ (28% vs. 8%), PKC (30% vs. 8%), and PKC (44% vs. 12%) (P Ͻ 0.05 in all cases) (Tables 3 and 4),'' should read: ''In estrogen-treated animals, these numbers were higher than in the oil group, ER␣ (66 vs. 20 estrogen ͉ hypothalamus ͉ lordosis ͉ oxytocin ͉ PKC E strogens, steroid sex hormones, play important roles in the development and establishment of reproductive and sexual behaviors as well as many other nonreproductive functions (1-4). Although estrogens' actions in females are relatively well understood, its role in male CNS function is less studied (5). Estrogens are regulated by binding to specific nuclear estrogen receptors (ERs), ER␣ and ER␤, ligand-activated transcription factors (6). ER␣ and ER␤ belong to a large group of six subfamilies of transcription factors (7), one of which comprises the steroid receptors (8). ER expression in the brain varies by region (9) and can affect both female and male sexual behaviors (10-12). Both ER␣ and ER␤ are expressed in the hypothalamus, and particularly in ventromedial nucleus (VMN), which is well known to regulate female sexual behavior (13,14).In addition to regulating sexual behaviors, estrogens affect affiliative social behaviors by affecting mRNA levels for the oxytocin receptors (OTR) (15), which are expressed in VMN (4,(16)(17)(18)(19). Regulation of OTR by estrogens in VMN has been shown in females as well as males (16,18,(20)(21)(22)(23)(24)(25). A four-gene micronet theory featuring ER␣, ER␤, oxytocin, and OTR and has been proposed to explain how neurons in hypothalamus and amygdala cooperate to facilitate social behaviors in female rodents (26,27). OTRs are important for sex and anxiety behaviors (4). Regulation of OTR also requires second messenger-mediated kinases (28), one of which involves PKCs (29). Evidence shows that PKC␣ associates with OTR within 2 min of agonist stimulation (30).It has been demonstrated that estrogens have two types of actions: genomic and membrane (31-33). Although ERs play a major role in genomic actions of estrogens, nongenomic actions in neurons involve several signal transduction pathways (34). And although lordosis behavior requires genomic actions of estrogens in VMN (35), estrogen-induced membrane actions in VMN can potentiate these genomic actions in a manner involving PKC (14). Several in vitro studies show that activation of PKC is involved in the potentiating effect of the rapid membrane actions of estrogens (34,(36)(37)(38)(39). PKCs comprise a family of 12 related isozymes (40) that are divided into three groups: classical or calcium-dependent (PKC␣, -␤I, -␤II, and -␥); the n...

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“…All experiments used female Sprague Dawley rats (225-250 gm; Bantin-Kingman, Hull, UK) maintained under standard animal housing conditions, including a 14/10 hr light/dark illumination cycle (lights on at 5:00 A.M.). Because ovarian steroid variations occurring over the estrous cycle could influence oxytocin and oxytocin receptor expression (de Kloet et al, 1985;Patchev et al, 1993;Krémarik et al, 1995), each rat underwent bilateral ovariectomy and simultaneous implantation of a SILASTIC capsule (1.6 mm inner diameter; 10 mm length/100 gm body weight) containing 150 g of 17␤ estradiol benzoate per milliliter of vegetable oil. This is known to produce estradiol concentrations within the normal diestrus range (Goodman, 1978).…”

Section: Methodsmentioning

confidence: 99%

Oxytocin Attenuates Stress-Induced c-fosmRNA Expression in Specific Forebrain Regions Associated with Modulation of Hypothalamo–Pituitary–Adrenal Activity

Windle¹,

Kershaw²,

Shanks³

et al. 2004

J. Neurosci.

379

288

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We reported previously that the neuropeptide oxytocin attenuates stress-induced hypothalamo-pituitary-adrenal (HPA) activity and anxiety behavior. This study sought to identify forebrain target sites through which oxytocin may mediate its anti-stress effects. Ovariectomized, estradiol-treated rats received intracerebroventricular infusions of oxytocin (1 or 10 ng/hr) or vasopressin (10 ng/hr), and the patterns of neuronal activation after restraint stress were determined by semiquantitative mapping of c-fos mRNA expression. Oxytocin administration significantly attenuated the release of ACTH and corticosterone and the increase in corticotropin-releasing factor mRNA expression in the hypothalamic paraventricular nucleus (PVN) in response to 30 min restraint. Restraint also induced the expression of c-fos mRNA in selective regions of the forebrain, including the PVN, paraventricular thalamic nucleus, habenula, medial amygdala, ventrolateral septum (LSV), most subfields of the dorsal and ventral hippocampus, and piriform and endopiriform cortices. In most cases, this level of gene expression was unaffected by concomitant administration of oxytocin. However, in the PVN, LSV, and throughout all subfields of the dorsal hippocampus, restraint evoked no detectable increase in c-fos mRNA in animals treated with either dose of oxytocin. Vasopressin had no effects on either HPA axis responses or neuronal activation in response to restraint, indicating that the effects were highly peptide selective. These data show that central oxytocin attenuates both the stress-induced neuroendocrine and molecular responses of the HPA axis and that the dorsal hippocampus, LSV, and PVN constitute an oxytocin-sensitive forebrain stress circuit.

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Estradiol induces oxytocin binding sites in rat hypothalamic ventromedial nucleus

Cited by 124 publications

References 4 publications

Electrophysiological Actions of Oxytocin on Hypothalamic Neurons in vitro: Neuropharmacological Characterization and Effects of Ovarian Steroids

Electrophysiological Actions of Oxytocin on Hypothalamic Neurons in vitro: Neuropharmacological Characterization and Effects of Ovarian Steroids

Sex and estrogenic effects on coexpression of mRNAs in single ventromedial hypothalamic neurons

Oxytocin Attenuates Stress-Induced c-fosmRNA Expression in Specific Forebrain Regions Associated with Modulation of Hypothalamo–Pituitary–Adrenal Activity

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