Endocrine disrupting effects of estrone on male Siniperca chuatsi: From gonadal remodeling to gene regulation.

Abstract

Estrone (E1), a ubiquitous environmental estrogen, poses a potential threat to the reproductive health of aquatic organisms. To evaluate the inducing effect of E1 exposure on gonadal feminization in male Siniperca chuatsi, male fish were exposed to 0, 0.01, 0.1, and 1 μg/L E1 for 60 days. The effects of E1 exposure on serum sex hormones, gonadal histological sections, vasa in situ hybridization, cell apoptosis, and gene expression in S. chuatsi were systematically examined. The results showed that 0.1 μg/L E1 treatment significantly inhibited testicular germ cell development, while 1 μg/L E1 treatment induced gonad histological feminization in 80% of male fish, with early vitellogenic oocytes appeared. Additionally, E1 exposure caused significant changes in serum sex hormones: 11-ketotestosterone levels significantly decreased, while immunoreactive estradiol levels significantly increased. Vasa gene in situ hybridization showed positive signals and TUNEL cell apoptosis revealed no obvious apoptotic signals in E1-induced histologically feminized gonads. Further molecular analysis revealed that sex regulation and development-related genes were involved in the E1-mediated gonadal feminization process: the expression of key male sex determination genes (dmrt1, amh, gsdf, sox9) and steroidogenic support genes (star, fshr) was significantly down-regulated, while expression of key female differentiation genes (bmp15, foxl2, cyp19a1a, hsd17b1) and germ cell development genes (sox19a, dazl, vasa, ccne2, sox3) was significantly up-regulated. Collectively, these findings demonstrate that E1 exposure induces histological testicular feminization in male S. chuatsi in a dose-dependent manner, concomitant with transcriptional downregulation of male differentiation genes and upregulation of female differentiation genes.