Insulin-like growth factors 1 and 2 regulate gene expression and enzymatic activity of cyp17a1 in ovarian follicles of the yellowtail, Seriola quinqueradiata

Kentaro Higuchi,Yukinori Kazeto,Yuichi Ozaki,Daisuke Izumida,Takuro Hotta,Kiyoshi Soyano,Koichiro Gen

doi:10.1016/j.heliyon.2020.e04181

Kentaro Higuchi, Yukinori Kazeto + Show 5 more

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https://doi.org/10.1016/j.heliyon.2020.e04181

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Journal: Heliyon	Publication Date: Jun 1, 2020
Citations: 10	License type: cc-by

Affiliation: Fisheries Research Agency, Nagasaki University

Abstract

There is accumulating evidence that insulin-like growth factors (IGFs), primary mediators of somatic growth, play an important role in fish reproduction. Previously, we showed that IGF-1 and IGF-2 are expressed in the ovarian follicle cells of the yellowtail (Seriola quinqueradiata) during the vitellogenic phase, suggesting that IGFs may be involved in ovarian steroidogenesis. In this study, we examined the effects of IGF-1 and IGF-2 on gene expression and activity of steroidogenic enzymes in yellowtail ovary in vitro. IGF-1 and IGF-2 had no effect on mRNA levels of several steroidogenesis-related genes (star, cyp11a1, hsd3b, cyp17a2, and cyp19a1). However, both IGFs enhanced the transcription of cyp17a1 in vitellogenic ovaries, although such up-regulation was not found in the ovary at the pre-vitellogenic stage. The stage-dependent effects of IGFs were correlated with changes in ovarian cyp17a1 mRNA levels during the reproductive cycle: transcript abundances increased in conjunction with ovarian development. In addition, IGF-induced cyp17a1 gene expression was significantly inhibited by wortmannin, suggesting that PI3 kinase plays an essential role in IGF-mediated ovarian steroidogenesis. Furthermore, IGF-1 and IGF-2 promoted the conversion of both progesterone and 17α-hydroxyprogesterone to androstenedione in vitellogenic ovaries, suggesting that both IGFs stimulated 17α-hydroxylase and C17-20 lyase activities. Taken together, these findings suggest that IGF-1 and IGF-2 act directly on follicle cells to stimulate steroid production through an increase in gene expression and enzymatic activity of cyp17a1 via induction of PI3 kinase.

Highlights

Insulin-like growth factors (IGFs: IGF-1 and IGF-2), primary mediators of somatic growth, play essential roles in gonadal development and maturation in a wide variety of vertibrates
To gain a better understanding of the various physiological roles of IGFs in fish reproduction, we examined the regulatory roles of IGF-1 and IGF-2 for the gene expression and activity of steroidogenic enzymes in ovaries of our model fish species, the yellowtail, which is known as a multiple-spawner with an asynchronous-type ovary (Matsuyama et al, 1996)
We demonstrated that IGF-1 and IGF-2 could stimulate only cyp17a1 gene expression in the yellowtail ovary in vitro

Summary

Introduction

Insulin-like growth factors (IGFs: IGF-1 and IGF-2), primary mediators of somatic growth, play essential roles in gonadal development and maturation in a wide variety of vertibrates. IGFs have been shown to affect gonadal steroidogenesis, differentiation and proliferation of somatic cells in the gonads, and be involved in oocyte maturation (Bondy et al, 2006). IGF-1 has been shown to potentiate the stimulatory effects of gonadotropins on steroid production and expression of steroidogenic enzymes in mammalian theca cells (Bondy et al, 2006). As in mammals, IGF-1 stimulates steroid production in the ovarian follicles. Both IGF-1 and IGF-2 induce maturational competence and final oocyte maturation (Reinecke, 2010). Fish IGFs are primarily produced in the liver and exert their actions in various tissues to induce growth, proliferation, and differentiation of peripheral tissues via the blood stream (Reindl and Sheridan, 2012). IGFs as well as their receptors are expressed in the ovary of teleosts, such as the zebrafish (Danio rerio) (Zhou et al, 2016), coho salmon (Oncorhynchus kisutch) (Maestro et al, 1997), common carp (Cyprinus carpio)

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