Duplicated membrane estrogen receptors in the European sea bass (Dicentrarchus labrax): Phylogeny, expression and regulation throughout the reproductive cycle

Abstract

The numerous estrogen functions reported across vertebrates have been classically explained by their binding to specific transcription factors, the nuclear estrogen receptors (ERs). Rapid non-genomic estrogenic responses have also been recently identified in vertebrates including fish, which can be mediated by membrane receptors such as the G protein-coupled estrogen receptor (Gper). In this study, two genes for Gper, namely gpera and gperb, were identified in the genome of a teleost fish, the European sea bass. Phylogenetic analysis indicated they were most likely retained after the 3R teleost-specific whole genome duplication and raises questions about their function in male and female sea bass. Gpera expression was mainly restricted to brain and pituitary in both sexes while gperb had a widespread tissue distribution with higher expression levels in gill filaments, kidney and head kidney. Both receptors were detected in the hypothalamus and pituitary of both sexes and significant changes in gpers expression were observed throughout the annual reproductive season. In female pituitaries, gpera showed an overall increase in expression throughout the reproductive season while gperb levels remained constant. In the hypothalamus, gpera had a higher expression during vitellogenesis and decreased in fish entering the ovary maturation and ovulation stage, while gperb expression increased at the final atresia stage. In males, gpers expression was constant in the hypothalamus and pituitary throughout the reproductive cycle apart from the mid- to late testicular development stage transition when a significant up-regulation of gpera occurred in the pituitary. The differential sex, seasonal and subtype-specific expression patterns detected for the two novel gper genes in sea bass suggests they may have acquired different and/or complementary roles in mediating estrogens actions in fish, namely on the neuroendocrine control of reproduction.

Cartography of rhodopsin-like G protein-coupled receptors across vertebrate genomes

“…A new subtype in ray-fin fishes (8) has been previously reported, which may be a fish-specific duplicate (3R) 90 .…”

Role of estrogens in fish immunity with special emphasis on GPER1

“…In fish, GPER1 has been described in Atlantic croaker (Pang et al, 2008), zebrafish (Liu et al, 2009), goldfish (Mangiamele et al, 2017), gilthead seabream (Cabas et al, 2013), common carp (Majumder et al, 2015), and orange-spotted grouper (Epinephelus coioides) (Nagarajan et al, 2011). Interestingly, two GPER genes, gpera and gperb, have recently been identified in the: (i) reproductive tissues of European eel, where they have a different tissue distribution and regulation in response to experimentally-induced maturation in both sexes (Morini et al, 2017), and (ii) European sea bass, where gpera expression is mainly restricted to brain and pituitary in both sexes while gperb has a widespread tissue distribution, with higher expression levels in gill, kidney and head kidney (Pinto et al, 2017). Despite the presence of GPER1 in fish, to date, this receptor has mainly been linked with oocyte maturation (Pang et al, 2008;Pang and Thomas, 2009), brain development (Shi et al, 2013) and embryonic heart rate (Romano et al, 2017).…”

Genistein and estradiol have common and specific impacts on the sea bass (Dicentrarchus labrax) skin-scale barrier

“…The expression of nuclear Esrs at both transcript and protein levels explains the responsiveness of fish scales to (E2 [3,[6][7][8]. Recently, duplicate Gper paralogues were found to be expressed in European sea bass (Dicentrarchus labrax) and Mozambique tilapia (Oreochromis mossambicus) scales [7][8][9] indicating that fish scales are estrogen targets through both classical genomic actions and rapid non-genomic actions [3].…”