How does oestradiol influence the AVT/IT system in female round gobies during different reproductive phases?

Abstract

In this in vitro gradient perfusion study, we determined whether there is a functional relationship between oestradiol and the arginine vasotocin/isotocin (AVT/IT) system in the female round goby (Neogobius melanostomus). Brain explants were perfused in medium supplemented with 17β-oestradiol (E2) at doses mimicking the plasma levels of this hormone in nature during the spawning-capable phase and regressing phase. We aimed to establish which pathway, genomic or non-genomic, is involved in this mechanism in different reproductive phases. For this purpose, brain explants were perfused in medium supplemented with Fulvestrant (ICI 182.780) or Actinomycin D (Act D) separately or in combination with E2. The contents of AVT and IT in the perfusion media were determined using high-performance liquid chromatography (HPLC) with fluorescence and UV detection. During the spawning-capable phase, the effect of E2 on AVT release is mediated through oestrogen receptors (ERs) via both genomic and non-genomic pathways, while IT release is mediated through ERs via a genomic pathway only. In the regressing phase, release of both nonapeptides is mediated through ERs via a genomic pathway. This is the first study to present a feasible mechanism of oestradiol action on the AVT/IT system in female fish during different phases of the reproductive cycle.

Reproductive roles of the vasopressin/oxytocin neuropeptide family in teleost fishes

“…The results show that high Avp levels correlate with pre-spawning period whereas the highest Oxt levels correspond to spawning. In female round gobies, these increases appear, at least in part, to be dependent on estrogens acting via genomic (nuclear receptors), and genomic and non-genomic mechanisms in the case of Avp and Oxt, respectively ( 98 ). This suggests that season-dependent gonadally-derived positive sex steroid feedback mechanisms may reinforce the seasonal activation of hypothalamic nonapeptide systems.…”

“…This regulation also appears to be indirect, as androgen receptor expression was not found in Oxt neurons but on kisspeptin neurons known to stimulate Oxt neurons in this species ( 131 , 135 ). In female round gobies, circulating E 2 levels are higher in the spawning phase compared to non-spawning phase and coincide with high circulating Avp and Oxt concentrations ( 98 ). Brain explant exposure to E 2 in spawning and non-spawning phases stimulated Avp and Oxt release in this species; however, pharmacological studies using the estrogen receptor (ER) antagonist fulvestrant and the transcription inhibitor actinomycin D showed that the effect of E 2 on Avp and Oxt release was mediated by different signaling pathways ( 98 ).…”

Female reproductive state is associated with changes in distinct arginine vasotocin cell types in the preoptic area of Astatotilapia burtoni

“…This suggests that in females, AVT production may be associated with physiological status and egg development, ovulation, and steroid hormone production. Further, in female round gobies, perfusion with 17β‐estradiol over explanted brains increased AVT release, and acted through both genomic and nongenomic pathways (Kalamarz‐Kubiak et al, 2017), and gonadal steroids, particularly estrogens, mediate AVT production and expression across taxa (Boyd, 1994; Miller et al, 1989; Sladek & Somponpun, 2008). Gravid, ready‐to‐spawn A .…”

“…While many studies documented the presence or absence of sexually dimorphic AVT expression and immunoreactivity, these studies have largely grouped females into a single category while separating males by reproductive or social status. However, gonadal steroids, especially estradiol help maintain and regulate AVT/AVP levels in the brains of fishes, amphibians, and mammals (Boyd, 1994; Kalamarz‐Kubiak, Gozdowska, Guellard, & Kulczykowska, 2017; Miller, Urban, & Dorsa, 1989; Sladek & Somponpun, 2008), suggesting that female reproductive state regulates AVT expression and production. Thus, it is important to examine plasticity of the AVT system in females, as they also undergo cyclical changes in behaviors (aggressive, reproductive, parental) and reproductive physiology comparable to males in many species.…”

Effect of short-term intermittent exposure to waterborne estradiol on the reproductive physiology of the round goby (Neogobius melanostomus)

“…Plasma E 2 was measured using RIA kit (ESTR-CTRIA, Cisbio Bioassays, Codolet, France) without preceding extraction procedure according to the manufacturer’s protocol validated in our laboratory (Kalamarz-Kubiak et al 2017 ; Guellard et al 2019 ). E 2 iodinated with 125 I was used as a tracer.…”