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苯并[a]芘暴露对性逆转海马(直立海马)卵巢、睾丸和育儿袋的生殖毒性及分子机制

Reproductive toxicity and molecular mechanisms of benzo[a]pyrene exposure on ovary, testis, and brood pouch of sex-role-reversed seahorses (Hippocampus erectus).

作者信息

Xue Yuanyuan, Wang Fang, Su Xiaolei, Li Mingzhu, Yan Hansheng, Zheng Shiyi, Ma Yicong, Dong Jie, Liu Yali, Lin Qiang, Wang Kai

机构信息

School of Fisheries, Ludong University, Yantai, 264025, China; Research and Development Center of Science, Technology and Industrialization of Seahorses, Ludong University, Yantai, 264025, China.

Department of Pathology, The Affiliated Yantai Yuhuangding Hospital of Qingdao University, Yantai, 264025, China.

出版信息

Environ Pollut. 2025 Feb 15;367:125569. doi: 10.1016/j.envpol.2024.125569. Epub 2024 Dec 21.

DOI:10.1016/j.envpol.2024.125569
PMID:39716499
Abstract

As a flagship taxa for marine ecosystems, seahorses possess a unique reproductive strategy of "male pregnancy". They are severely threatened by marine petroleum-based pollution but the molecular mechanism involved remains unclear. We evaluated the toxic effects and mechanisms of sub-acute exposure to benzo[a]pyrene (BaP), a representative polycyclic aromatic hydrocarbon (PAH), at three environmental related dosages (0.5, 5, and 50 μg/L) on the reproductive organs of sex-role-reversed lined seahorses (Hippocampus erectus). BaP induced ovary, testis and brood pouch tissue damage in a concentration-dependent manner. Transcriptomic results suggested that reproductive organs of the seahorse could undergo biotransformation and detoxification of BaP via the P450 enzyme system; the differential expression of key genes related to these pathways determined the differences in the accumulation of toxic substances in the reproductive organs. Moreover, toxic substances directly induced differential tissue damage in situ by activating tissue-specific signaling pathways: BaP-induced ovarian apoptosis and failure by upregulation of the pro-apoptotic genes, vadc1, traf2b, tnfsf10, and pycard (P < 0.05); inhibition of testicular function through disruption of genes associated with "ECM-receptor interaction", "Tight junction", and "Spermatogenesis" pathways; and interference with brood pouch immune responses, significantly suppressing the expression of ripk1, il-1b, casp3a, apaf1, calr, and canx (P < 0.05), thereby impairing "Apoptosis", "Phagosome", and "Necroptosis" processes, ultimately compromising brood pouch maintenance. Toxic substances exacerbate damage to the reproductive organs in seahorses by disrupting Ca homeostasis. At environmentally-relevant concentrations of BaP, the reproductive efficiency of seahorses may be severely affected, increasing the risk of a decline in the abundance and diversity of wild populations.

摘要

作为海洋生态系统的旗舰物种,海马具有独特的“雄性怀孕”繁殖策略。它们受到海洋石油污染的严重威胁,但其中涉及的分子机制仍不清楚。我们评估了亚急性暴露于三种环境相关剂量(0.5、5和50μg/L)的代表性多环芳烃(PAH)苯并[a]芘(BaP)对性别角色反转的斑纹海马(Hippocampus erectus)生殖器官的毒性作用和机制。BaP以浓度依赖的方式诱导卵巢、睾丸和育儿袋组织损伤。转录组学结果表明,海马的生殖器官可通过P450酶系统对BaP进行生物转化和解毒;与这些途径相关的关键基因的差异表达决定了生殖器官中有毒物质积累的差异。此外,有毒物质通过激活组织特异性信号通路直接在原位诱导不同的组织损伤:BaP通过上调促凋亡基因vadc1、traf2b、tnfsf10和pycard诱导卵巢凋亡和功能衰竭(P<0.05);通过破坏与“细胞外基质-受体相互作用”、“紧密连接”和“精子发生”途径相关的基因来抑制睾丸功能;干扰育儿袋免疫反应,显著抑制ripk1、il-1b、casp3a、apaf1、calr和canx的表达(P<0.05),从而损害“凋亡”、“吞噬体”和“坏死性凋亡”过程,最终影响育儿袋的维持。有毒物质通过破坏钙稳态加剧对海马生殖器官的损害。在与环境相关的BaP浓度下,海马的繁殖效率可能会受到严重影响,增加野生种群数量和多样性下降的风险。

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