Temperature modulates 17β-estradiol regulation of oogenesis protein expression in the liver of the eurythermal pupfish Cyprinodon nevadensis

Abstract

Female fish experiencing atypically high or prolonged elevations in temperature during oogenesis can suffer impaired oocyte development with fewer or smaller eggs, eggs with reduced yolk content or thinner envelopes, and lower egg viability. These changes in oocyte quality and quantity are in part caused by diminished liver synthesis of egg yolk (vitellogenin, Vtg) and egg envelope (choriogenin) proteins at anomalously high temperatures. Those declines in liver Vtg and choriogenin production are commonly paralleled by reduced blood concentrations of 17β-estradiol (E₂). However, it is unclear whether declines in liver vitellogenin and choriogenin production at elevated temperatures result solely from lower circulating E₂ or if other aspects of E₂ signaling are also altered to diminish liver synthesis of oogenesis proteins. In this study, adult female Amargosa River pupfish (Cyprinodon nevadensis amargosae), a species with asynchronous follicular development, were maintained at 20 °C, 28 °C, or 36 °C and then administered E₂ or vehicle solution. Ovarian gonadosomatic index (GSI) values and plasma E₂ were lower in females at 36 °C compared to those at cooler temperatures. Females at 36 °C also had reduced plasma Vtg protein, lower liver abundances for mRNAs encoding vitellogenin genes (vtgAa, vtgAb, vtgc), choriogenin genes (cgh, cghm, cgl), and estrogen receptor α (esr1). Supplemental E₂ increased plasma E₂ in females at all temperatures, but only upregulated liver vitellogenin and choriogenin mRNAs at 36 °C, despite E₂ upregulation of hepatic esr1 receptor transcripts at all temperatures. Females at 36 °C also exhibited higher liver mRNA abundances for sex hormone-binding globulin (shbg) and cytochrome P450 family 1 subfamily A member 1 (cyp1a1), an estrogen-metabolizing monooxygenase enzyme that converts E₂ to 2-hydroxyestradiol. Together, these findings indicate elevated temperatures diminish E₂ stimulation of liver Vtg and choriogenin expression in pupfish via effects on several aspects of E₂ signaling including circulating E₂ concentrations and liver esr1 expression as well as shbg and cyp1a1 expression, which may result in changes to free:bound E₂ and the rate of hepatic E₂ inactivation. These results also demonstrate that E₂ replacement can help compensate for high temperature-induced declines in hepatic oogenesis gene expression in female pupfish.