GPER/GPR30, a membrane estrogen receptor, is expressed in the brain and retina of a social fish (Carassius auratus) and colocalizes with isotocin

Abstract

Estradiol rapidly (within 30 minutes) influences a variety of sociosexual behaviors in both mammalian and nonmammalian vertebrates, including goldfish, in which it rapidly stimulates approach responses to the visual cues of females. Such rapid neuromodulatory effects are likely mediated via membrane-associated estrogen receptors; however, the localization and distribution of such receptors within the nervous system is not well described. To begin to address this gap, we identified GPER/GPR30, a G-protein-coupled estrogen receptor, in goldfish (Carassius auratus) neural tissue and used reverse-transcription polymerase chain reaction (RT-PCR) and in situ hybridization to test if GPR30 is expressed in the brain regions that might mediate visually guided social behaviors in males. We then used immunohistochemistry to determine whether GPR30 colocalizes with isotocin-producing cells in the preoptic area, a critical node in the highly conserved vertebrate social behavior network. We used quantitative (q)PCR to test whether GPR30 mRNA levels differ in males in breeding vs. nonbreeding condition and in males that were socially interacting with a female vs. a rival male. Our results show that GPR30 is expressed in the retina and in many brain regions that receive input from the retina and/or optic tectum, as well as in a few nodes in the social behavior network, including cell populations that produce isotocin.

Steroid Transport, Local Synthesis, and Signaling within the Brain: Roles in Neurogenesis, Neuroprotection, and Sexual Behaviors

“…G protein-coupled estrogen receptor 1 (GPER or GPR30) is a member of this receptor family. A partial or full-length gper was cloned, characterized, and detected in the brain of adult zebrafish, Atlantic croaker, and goldfish (Pang et al, 2008 ; Liu et al, 2009 ; Pang and Thomas, 2009 ; Mangiamele et al, 2017 ). In zebrafish, gper in situ hybridization on adult brain sections showed a specific pattern of expression in the olfactory bulbs, the telencephalon, the hypothalamus, the optic tectum, the cerebellum, and the medulla oblongata (Liu et al, 2009 ).…”

“…In zebrafish, gper in situ hybridization on adult brain sections showed a specific pattern of expression in the olfactory bulbs, the telencephalon, the hypothalamus, the optic tectum, the cerebellum, and the medulla oblongata (Liu et al, 2009 ). In goldfish, gper was also expressed in the forebrain and the suprachiasmatic nucleus, the preoptic area, and the optic tectum (Mangiamele et al, 2017 ). Originally, it was proposed that goldfish RGCs did not express the G-protein coupled estrogen receptor because attempts to amplify a specific cDNA from cultured cells failed (Xing et al, 2015 ).…”

Neurodevelopmental effects of natural and synthetic ligands of estrogen and progesterone receptors in zebrafish eleutheroembryos

“…Estrogen and progesterone effects in the brain could also be mediated through membrane steroid receptors (Hanna and Zhu, 2009;Liu et al, 2009;Mangiamele et al, 2017;Zhang et al, 2016;Zhu et al, 2003). Membrane progesterone receptors (mPRs) are abundantly expressed in different areas of the brain of fish including zebrafish (Hanna and Zhu, 2009;Zhang et al, 2016;Zhu et al, 2003) and GPER is described in olfactory bulbs, telencephalon, optic tectum, hypothalamus, cerebellum and medulla oblongata (Liu et al, 2009).…”

Effects of Sex Steroids on Fish Leukocytes

“…In fish, European eel show two G-protein coupled oestrogen receptors (GPER: GPERa and GPERb) in reproductive tissues [ 108 ]. Although two GPERs are expected in most fish species as a consequence of genome duplication events that have occurred in fish, only one GPER has been characterized in most of the species studied, such as goldfish, gilthead seabream, Atlantic croaker, zebrafish, common carp and orange-spotted grouper ( Epinephelus coioides ) [ 7 , 99 , 109 , 110 , 111 , 112 ]. In gilthead seabream, GPER is expressed in acidophilic granulocytes but also in other leukocytes such as spleen and peritoneal leukocytes [ 89 , 109 ], although the correct identification of these leukocytes needs further studies.…”