Oestradiol Potentiates Hormone Secretion and Neuronal Activation in Response to Hypertonic Extracellular Volume Expansion in Ovariectomised Rats

Abstract

Secretion of vasopressin (VP), oxytocin (OT) and atrial natriuretic peptide (ANP) is an essential mechanism for the maintenance of hydromineral homeostasis. Secretion of these hormones is modulated by several circulating factors, including oestradiol. However, it remains unclear how oestradiol exerts this modulation. In the present study we investigated the participation of oestradiol in the secretion of VP, OT and ANP and in activation of vasopressinergic and oxytocinergic neurones of the supraoptic (SON) and paraventricular (PVN) nuclei of the hypothalamus in response to extracellular volume expansion (EVE). For this purpose, ovariectomised (OVX) rats treated for 7 days with vehicle (corn oil, 0.1 ml/rat, OVX+O group) or oestradiol (oestradiol cypionate, 10 μg/kg, OVX+E group) were subjected to either isotonic (0.15 m NaCl, 2 ml/100 g b.w., i.v.) or hypertonic (0.30 m NaCl, 2 ml/100 g b.w., i.v.) EVE. Blood samples were collected for plasma VP, OT and ANP determination. Another group of rats was subjected to cerebral perfusion, and brain sections were processed for c-Fos-VP and c-Fos-OT double-labelling immunohistochemistry. In OVX+O rats, we observed that both isotonic and hypertonic EVE increased plasma OT and ANP concentrations, although no changes were observed in VP secretion. Oestradiol replacement did not alter hormonal secretion in response to isotonic EVE, but it increased VP secretion and potentiated plasma OT and ANP concentrations in response to hypertonic EVE. Immunohistochemical data showed that, in the OVX+O group, hypertonic EVE increased the number of c-Fos-OT and c-Fos-VP double-labelled neurones in the PVN and SON. Oestradiol replacement did not alter neuronal activation in response to isotonic EVE, but it potentiated vasopressinergic and oxytocinergic neuronal activation in the medial magnocellular PVN (PaMM) and SON. Taken together, these results suggest that oestradiol increases the responsiveness of vasopressinergic and oxytocinergic magnocellular neurones in the PVN and SON in response to osmotic stimulation.

Estradiol potentiates hypothalamic vasopressin and oxytocin neuron activation and hormonal secretion induced by hypovolemic shock

“…However, despite previous demonstrations of the colocalization of estrogen and ANP receptors in cardiomyocytes and ANP secretion induced by estrogen perfusion in atrial cardiac cells, we did not observe an influence of estrogen on ANP secretion under basal or hemorrhagic conditions (4,19). Although estrogen was shown to modulate ANP secretion in response to osmolality changes and extracellular volume expansion (66), it seems that the reduction of ANP release during hemorrhage is not influenced by estrogen treatment.…”

Effect of the interaction between food state and the action of estrogen on oxytocinergic system activity

“…Adult rats release AVP and OT in response to osmotic stimuli even in the presence of circulating estrogen (Caligioni & Franci 2002, Vilhena-Franco et al 2011. The downregulation of ER-b during hyperosmolality may remove this inhibitory influence, allowing the release of AVP and OT in situations that require maximum secretion.…”

“…FOS expression has been reliably used to assess brain activity in response to food intake (Naimi et al 1997, Timofeeva et al 2002. It is also known that OT and AVP neurones in the PVN and the SON express FOS in response to an increase in osmolality , Ruginsk et al 2007, Vilhena-Franco et al 2011. Timofeeva et al (2005) have shown that AVP neurones, but not OT neurones, respond to refeeding.…”

Mapping and signaling of neural pathways involved in the regulation of hydromineral homeostasis

“…Furthermore, several studies have proposed a stimulatory role for estradiol on OT and ANP secretion 85,86. More recently, the contribution of estradiol to AVP, OT and ANP secretion as well as to vasopressinergic and oxytocinergic neuronal activation has been demonstrated 87,88. Estradiol has been shown to positively modulate AVP and OT secretion in response to osmotic stimulation induced by hypertonic extracellular volume expansion 87 and hypovolemic shock 88, without altering ANP secretion.…”

“…More recently, the contribution of estradiol to AVP, OT and ANP secretion as well as to vasopressinergic and oxytocinergic neuronal activation has been demonstrated 87,88. Estradiol has been shown to positively modulate AVP and OT secretion in response to osmotic stimulation induced by hypertonic extracellular volume expansion 87 and hypovolemic shock 88, without altering ANP secretion. These same studies also showed that the activity of both oxytocinergic and vasopressinergic neurons in the SON and PVN may be modulated by estradiol.…”