Benzo[a]pyrene exposure induced reproductive endocrine-disrupting effects via the steroidogenic pathway and estrogen signaling pathway in female scallop Chlamys farreri

Abstract

Benzo[a]pyrene (B[a]P), as one of the typical polycyclic aromatic hydrocarbons and environmental contaminants, may cause endocrine disrupting effects and reproductive impairments in bivalves. However, the molecular mechanisms are still not fully understood. In this study, three reproductive stages (proliferative stage, growing stage and mature stage) of female scallops Chlamys farreri were exposed to B[a]P at 0, 0.38 and 3.8 μg/L. The present study determined the adverse effects of B[a]P on gonadosomatic index, circulating hormone concentrations, endocrine-associated gene expression and ovarian histology. Significant decrease in sex hormones including progesterone (P), testosterone (T) and 17β-estradiol (E2), was observed in B[a]P-treated C. farreri at growing stage and mature stage. These effects were associated with down-regulated expression of steroidogenic enzymes, including 3β-HSD, CYP17 and 17β-HSD, which were regulated by the upstream adenylate cyclase (Adcy) - protein kinase (PKA) signaling pathway. Ovarian transcript levels of estrogen receptor (ER) and caveolin-1 (cav-1) were decreased in B[a]P-treated C. farreri. Vitellogenin (Vtg), an estrogen-mediated gene involved in ovarian development, was down-regulated by B[a]P. Furthermore, ovarian histology was investigated to clarify the impairment of B[a]P on ovaries at growing stage and mature stage. Overall, the present results elucidated the anti-estrogenic mechanisms along the steroidogenic pathway and estrogen signaling pathway for the stage-dependent endocrine-disrupting effects of B[a]P. This finding provides important information regarding to the underlying molecular mechanisms of B[a]P-induced endocrine disruption in different reproductive stages of bivalves. In addition, the adverse effects should be taken into concertation during protection of bivalves germplasm resources and comprehensive evaluation of ecological risks.

Keywords: Benzo[a]pyrene; Chlamys farreri; Estrogen signaling; Gonadal development; Reproductive endocrine-disruption; Steroidogenesis.