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

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 vitel...

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Main Authors: Kentaro Higuchi, Yukinori Kazeto, Yuichi Ozaki, Daisuke Izumida, Takuro Hotta, Kiyoshi Soyano, Koichiro Gen
Format: Article
Language:English
Published: Elsevier 2020-06-01
Series:Heliyon
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2405844020310252
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spelling doaj-1fb824c492e1488cb49d3a479430575b2020-11-25T02:57:45ZengElsevierHeliyon2405-84402020-06-0166e04181Insulin-like growth factors 1 and 2 regulate gene expression and enzymatic activity of cyp17a1 in ovarian follicles of the yellowtail, Seriola quinqueradiataKentaro Higuchi0Yukinori Kazeto1Yuichi Ozaki2Daisuke Izumida3Takuro Hotta4Kiyoshi Soyano5Koichiro Gen6Seikai National Fisheries Research Institute, Japan Fisheries Research and Education Agency, Taira-machi, Nagasaki 851-2213, Japan; Corresponding author.Kamiura Station, National Research Institute of Aquaculture, Japan Fisheries Research and Education Agency, Kamiura, Saiki, Oita 879-2602, JapanNational Research Institute of Aquaculture, Japan Fisheries Research and Education Agency, Tamaki, Mie 519-0423, JapanInstitute for East China Sea Research, Nagasaki University, Taira-machi, Nagasaki 851-2213, JapanGoto Station, Seikai National Fisheries Research Institute, Japan Fisheries Research and Education Agency, Tamanoura, Goto, Nagasaki 853-0508, JapanInstitute for East China Sea Research, Nagasaki University, Taira-machi, Nagasaki 851-2213, JapanSeikai National Fisheries Research Institute, Japan Fisheries Research and Education Agency, Taira-machi, Nagasaki 851-2213, JapanThere 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.http://www.sciencedirect.com/science/article/pii/S2405844020310252Cell biologyMolecular biologyPhysiologyAquacultureCell cultureReproductive hormone
collection DOAJ
language English
format Article
sources DOAJ
author Kentaro Higuchi
Yukinori Kazeto
Yuichi Ozaki
Daisuke Izumida
Takuro Hotta
Kiyoshi Soyano
Koichiro Gen
spellingShingle Kentaro Higuchi
Yukinori Kazeto
Yuichi Ozaki
Daisuke Izumida
Takuro Hotta
Kiyoshi Soyano
Koichiro Gen
Insulin-like growth factors 1 and 2 regulate gene expression and enzymatic activity of cyp17a1 in ovarian follicles of the yellowtail, Seriola quinqueradiata
Heliyon
Cell biology
Molecular biology
Physiology
Aquaculture
Cell culture
Reproductive hormone
author_facet Kentaro Higuchi
Yukinori Kazeto
Yuichi Ozaki
Daisuke Izumida
Takuro Hotta
Kiyoshi Soyano
Koichiro Gen
author_sort Kentaro Higuchi
title Insulin-like growth factors 1 and 2 regulate gene expression and enzymatic activity of cyp17a1 in ovarian follicles of the yellowtail, Seriola quinqueradiata
title_short Insulin-like growth factors 1 and 2 regulate gene expression and enzymatic activity of cyp17a1 in ovarian follicles of the yellowtail, Seriola quinqueradiata
title_full Insulin-like growth factors 1 and 2 regulate gene expression and enzymatic activity of cyp17a1 in ovarian follicles of the yellowtail, Seriola quinqueradiata
title_fullStr Insulin-like growth factors 1 and 2 regulate gene expression and enzymatic activity of cyp17a1 in ovarian follicles of the yellowtail, Seriola quinqueradiata
title_full_unstemmed Insulin-like growth factors 1 and 2 regulate gene expression and enzymatic activity of cyp17a1 in ovarian follicles of the yellowtail, Seriola quinqueradiata
title_sort insulin-like growth factors 1 and 2 regulate gene expression and enzymatic activity of cyp17a1 in ovarian follicles of the yellowtail, seriola quinqueradiata
publisher Elsevier
series Heliyon
issn 2405-8440
publishDate 2020-06-01
description 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.
topic Cell biology
Molecular biology
Physiology
Aquaculture
Cell culture
Reproductive hormone
url http://www.sciencedirect.com/science/article/pii/S2405844020310252
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