Elsevier

Neuroscience

Volume 284, 22 January 2015, Pages 325-336
Neuroscience

Modulation of the activity of vasopressinergic neurons by estrogen in rats refed with normal or sodium-free food after fasting

https://doi.org/10.1016/j.neuroscience.2014.09.076Get rights and content

Highlights

  • Refeeding after fasting increases plasma osmolality and AVP levels.

  • Refeeding after fasting increases the activity of AVP neurons in the PVN and SON.

  • Estrogen modulates the activity of a subpopulation of AVP neurons directly in the lateral PVN.

  • Estrogen modulates the activity of AVP neurons indirectly through vMnPO.

  • Estrogen modulation on AVP neurons through vMnPO is at least in part via ERα.

Abstract

Feeding increases plasma osmolality and ovarian steroids may influence the balance of fluids. Vasopressin (AVP) neurons in the paraventricular nucleus (PVN) and supraoptic nucleus (SON) express estrogen receptor type β (ERβ), but not estrogen receptor type α (ERα). The circumventricular organs express ERα and project efferent fibers to the PVN and SON. Our aim was to assess whether interactions exist between food state-related osmolality changes and the action of estrogen on AVP neuron activity and estrogen receptor expression. We assessed plasma osmolality and AVP levels; fos-coded protein (FOS)- and AVP-immunoreactivity (-IR) and FOS-IR and ERα-IR in the median preoptic nucleus (MnPO) and organ vasculosum lamina terminalis (OVLT) in estrogen-primed and unprimed ovariectomized rats under the provision of ad libitum food, 48 h of fasting, and subsequent refeeding with standard chow or sodium-free food. Refeeding with standard chow increased plasma osmolality and AVP as well as the co-expression of FOS-IR/AVP-IR in the PVN and SON. These responses were not altered by estrogen, with the exception of the decreases in FOS-IR/AVP-IR in the lateral PVN. During refeeding, estrogen modulates only a subpopulation of AVP neurons in the lateral PVN. FOS-ERα co-expression in the ventral median preoptic nucleus (vMnPO) was reduced by estrogen and increased after refeeding with standard chow following fasting.

It appears that estrogen may indirectly modulate the activity of AVP neurons, which are involved in the mechanism affected by hyperosmolality-induced refeeding after fasting. This indirect action of estrogen can be at least in part via ERα in the vMnPO.

Introduction

Receptors of the central nervous system that detect changes in osmolality (osmoreceptors) are located mainly in the organum vasculosum of the lamina terminalis (OVLT), subfornical organ (SFO), and area postrema (AP) (Arima et al., 1998). The circumventricular organs (CVOs) have been suggested to be involved in monitoring alterations of plasma osmolality after both hyperosmotic challenge and feeding (Starbuck and Fitts, 2002, Hiyama et al., 2004). Conformational changes in osmoreceptor cells stimulate neurons in the supraoptic (SON) and paraventricular (PVN) nuclei, which secrete vasopressin (AVP) and oxytocin (OT). These hormones act on water, sodium, and chloride excretion mechanisms (Sladek and Knigge, 1977, Oliet and Bourque, 1993).

Plasma osmolality may increase after feeding or sodium intake (Bloom et al., 1975, Burlet et al., 1992). During feeding, the action of AVP contributes to controlling the balance of water and changes in blood pressure as well as ceasing food intake (Pittman et al., 1982, Palkovits, 1984, Langhans et al., 1991).

Estrogen may influence fluid balance by modulating the vasopressinergic and oxytocinergic systems (Caligioni and Franci, 2002, Somponpun, 2007). However, this action is not fully understood. Some studies have shown that estrogen has no significant effect on OT and AVP levels in the PVN (Van Tol et al., 1988, Crowley et al., 1993). Other researchers have demonstrated that estrogen treatment can reduce OT-mRNA levels in the PVN of previously ovariectomized rats (Shughrue et al., 2002). Studies involving double labeling in vivo, autoradiography, and immunohistochemistry have also shown that radiolabeled estrogen concentrates in OT and AVP neurons (Rhodes et al., 1981).

The expression of estrogen receptor subtype β (ERβ) in OT and AVP neurons has been well described in the literature (Hrabovszky et al., 1998, Laflame et al., 1998, Sladek and Somponpun, 2008). Estrogen may directly regulate AVP and OT secretion via ERβ; these receptors are expressed in both parvocellular and magnocellular neurons (Shughrue et al., 2002, Sladek and Somponpun, 2008). Indirect action of estrogen on OT and AVP neurons in rats via estrogen receptor subtype α (ERα) cannot be ruled out (Somponpum et al., 2004, Grassi et al., 2010) because the neurons of the MnPO and OVLT that express these receptors project to the SON (Voisin et al., 1997). In castrated rats, estrogen treatment either significantly reduces (Suzuki and Handa, 2004) or induces no change in (Greco et al., 2001) ERβ expression in the PVN. The disparity of these results may be due to differences in the doses of estrogen administered, the duration of treatment, or the amount of time between ovariectomy and treatment initiation. Changes in ER expression may alter the impact of gonadal steroids by amplifying or reducing the effects of increased ligand levels (Greco et al., 2001, Patisaul et al., 2001, Somponpun and Sladek, 2003, Suzuki and Handa, 2004).

Little is known regarding the mechanisms and pathways by which estrogen interferes with the activity of AVP neurons and with the liquid and electrolyte balance associated with the food state. Our aim was to analyze the interactions between food state-related changes in osmolality and the action of estrogen through ERα on the activity of AVP neurons.

Section snippets

Animals

The experimental protocols and animal manipulations followed the National Institutes of Health Guidelines for the Care and Use of Laboratory Animals and were approved by the Ethics Committee of the Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo. Female Wistar rats weighing 160–180 g were housed in individual cages under controlled temperature conditions (22 ± 1 °C) with a 12-h light–dark cycle and given free access to water and chow unless otherwise specified. Bilateral

Osmolality

Fig. 1A indicates that refeeding with standard chow increased plasma osmolality (mOsm/KgH2O). The osmolality in OVX rats treated with vehicle or estrogen and refed with standard chow after 48 h of fasting (313 ± 1.9 and 312 ± 1.5, respectively) was significantly higher than that of the ad libitum (303 ± 1.6 and 303 ± 1.7, respectively), 48-h-fasting (299 ± 1.1 and 301 ± 1.2, respectively), and sodium-free food-refed (305 ± 1.2 and 305 ± 1.8, respectively) animals (F3,160 = 26,29 p < 0.0001). No significant

Discussion

Our results revealed that osmolality increased by nearly 4% in ovariectomized animals treated with vehicle and refed with standard chow after 48 h of fasting; this increase was significantly different from the changes observed in the ad libitum, 48-h-fasting, and sodium-free food-refed animals. These results are consistent with previous studies, which have reported an increased plasma osmolality following refeeding or sodium intake (Houpt et al., 1983, Burlet et al., 1992, Gill et al., 1995).

Conclusion

Refeeding with standard chow after fasting increases osmolality and plasma AVP levels; FOS-AVP co-expression in the PaMM, PaML, and SON; and FOS-ERα co-expression in the vMnPO. Estrogen treatment did not alter these responses, with the exception of decreasing FOS-AVP co-expression in the PaML and FOS-ERα co-expression in the vMnPO. Therefore, it appears that estrogen may indirectly modulate the activity of AVP neurons involved in the mechanisms underlying refeeding-induced hyperosmolality

Funding

This work was supported by FAPESP (04/09638-9) and CNPq (300152/2010-8) from Brazil.

Acknowledgment

The authors are grateful to Marina Holanda for her technical support.

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