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苯并[a]芘暴露破坏类固醇生成并损害雄性扇贝(海湾扇贝)不同生殖阶段的精子发生。

Benzo[a]pyrene exposure disrupts steroidogenesis and impairs spermatogenesis in diverse reproductive stages of male scallop (Chlamys farreri).

机构信息

The Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, 266003, PR China.

The Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, 266003, PR China.

出版信息

Environ Res. 2020 Dec;191:110125. doi: 10.1016/j.envres.2020.110125. Epub 2020 Aug 27.

DOI:10.1016/j.envres.2020.110125
PMID:32861722
Abstract

Benzo[a]pyrene (BaP), a model compound of polycyclic aromatic hydrocarbon known to impair reproductive functions of vertebrates, while the data is scarce in marine invertebrates. To investigate the toxic effects of BaP on invertebrates reproduction, we exposed male scallop (Chlamys farreri) to BaP (0, 0.38 and 3.8 μg/L) throughout three stages of reproductive cycle (early gametogenesis stage, late gametogenesis stage and ripe stage). The results demonstrated that BaP decreased the gonadosomatic index and mature sperms counts in a dose-dependent manner. Significant changes in sex hormones contents and increased 17β-estradiol/testosterone ratio suggested that BaP produced the estrogenic endocrine effects in male scallops. In support of this view, we confirmed that BaP significantly altered transcripts of genes along the upstream PKA and PKC mediated signaling pathway like fshr, lhcgr, adcy, PKA, PKC, PLC and NR5A2. Subsequently, the expressions of genes encoding downstream steroidogenic enzymes (e.g., 3β-HSD, CYP17 and 17β-HSD) were impacted, which corresponded well with hormonal alterations. In addition, BaP suppressed transcriptions of spermatogenesis-related genes, including ccnd2, SCP3, NRF1 and AQP9. Due to different functional demands, these transcript profiles involved in spermatogenesis exhibited a stage-specific expression pattern. Furthermore, histopathological analysis determined that BaP significantly inhibited testicular development and maturation in male scallops. Overall, the present findings indicated that, playing as an estrogenic-like chemical, BaP could disrupt the steroidogenesis pathway, impair spermatogenesis and caused histological damages, thereby inducing reproductive toxicities with dose- and stage-specific effects in male scallops. And the adverse outcomes might threaten the stability of bivalve populations and destroy the function of marine ecosystems in the long term.

摘要

苯并[a]芘(BaP)是一种多环芳烃的模型化合物,已知会损害脊椎动物的生殖功能,而在海洋无脊椎动物中的数据却很少。为了研究 BaP 对无脊椎动物生殖的毒性作用,我们将雄性扇贝(Chlamys farreri)暴露于 BaP(0、0.38 和 3.8μg/L)中,贯穿生殖周期的三个阶段(早期配子发生阶段、晚期配子发生阶段和成熟阶段)。结果表明,BaP 以剂量依赖的方式降低了性腺指数和成熟精子计数。性激素含量的显著变化和 17β-雌二醇/睾酮比值的增加表明 BaP 对雄性扇贝产生了雌激素内分泌效应。支持这一观点,我们证实 BaP 显著改变了沿着上游 PKA 和 PKC 介导的信号通路的基因转录,如 fshr、lhcgr、adcy、PKA、PKC、PLC 和 NR5A2。随后,编码下游类固醇生成酶的基因(如 3β-HSD、CYP17 和 17β-HSD)的表达受到影响,这与激素变化很好地对应。此外,BaP 抑制了与精子发生相关的基因的转录,包括 ccnd2、SCP3、NRF1 和 AQP9。由于功能需求不同,这些与精子发生相关的转录谱表现出阶段特异性表达模式。此外,组织病理学分析确定 BaP 显著抑制了雄性扇贝的睾丸发育和成熟。总的来说,本研究结果表明,作为一种类雌激素化学物质,BaP 可以破坏类固醇生成途径,损害精子发生并导致组织学损伤,从而在雄性扇贝中产生剂量和阶段特异性的生殖毒性。这些不利后果可能会威胁双壳类种群的稳定性,并长期破坏海洋生态系统的功能。

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