Study on epigenotoxicity, sex hormone synthesis, and DNA damage of benzo[a]pyrene in the testis of male Ruditapes philippinarum

• Published in: The Science of the total environment Vol. 912; p. 169340
• Main Authors: Wang, Qiaoqiao, Tang, Jian, Pan, Luqing, Song, Aimin, Miao, Jingjing, Zheng, Xin, Li, Zeyuan
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 20.02.2024
• Subjects: cell proliferation; DNA damage; DNA damage repair; DNA methylation; environment; Epigenetic toxicity; males; Polycyclic aromatic hydrocarbons; Reproductive endocrine disruption; reproductive performance; reproductive toxicology; Ruditapes philippinarum; spermatids; spermatogenesis; steroid hormones; testes; Testis development; toxicity; Bcl-2; Testis development; 3β-HSD; CCNH; Reproductive endocrine disruption; XIAP; EGFR; UNG; DNMT; DNA damage repair; BRIP1; SCP2; Polycyclic aromatic hydrocarbons; PMS2; CYP17A; SH3GLB1; LHCGR; PRMT7; FANCJ; Ruditapes philippinarum; CDC6; DMRT; GnRHR; PPARγ; 5-HTR; BER; GNMT; MMR; FANCD2; FasL; FSHR; MCM3; CTNNB1; NER; SAH; TGFBI; LAMP; SAM; PFN2; Epigenetic toxicity
• ISSN: 0048-9697; 1879-1026
• DOI: 10.1016/j.scitotenv.2023.169340

Research on the mechanisms of reproductive toxicity caused by persistent organic pollutants (POPs) in marine animals has received significant attention. One group of typical POPs, called polycyclic aromatic hydrocarbons (PAHs), has been found to cause various reproductive toxicities in aquatic organisms, including epigenotoxicity, reproductive endocrine disruption, DNA damage effects and other reproductive toxicity, thereby affecting gonadal development. Interestingly, male aquatic animals are more susceptible to the disturbance and toxicity of environmental pollutants. However, current studies primarily focus on vertebrates, leaving a large gap in our understanding of the reproductive toxicity and mechanisms of PAHs interference in marine invertebrates. In this study, male Ruditapes philippinarum was used as an experimental subject to investigate reproduction-related indexes in clams under the stress of benzo[a]pyrene (B[a]P) at different concentrations (0, 0.8, 4 and 20 μg/L) during the proliferative, growth, maturity, and spawning period. We analyzed the molecular mechanisms of reproductive toxicity caused by PAHs in marine bivalves, specifically epigenotoxicity, reproductive endocrine disruption, and gonadal damage-apoptotic effect. The results suggest that DNA methylation plays a crucial role in mediating B[a]P-induced reproductive toxicity in male R. philippinarum. B[a]P may affect sex hormone levels, impede spermatogenesis and testis development in clams, by inhibiting the steroid hormone synthesis pathway and downregulating genes critical for cell proliferation, testis development, and spermatid expulsion. Moreover, the spermatids of male R. philippinarum were severely impaired under the B[a]P stress, leading to reduced reproductive performance in the clams. These findings contribute to a better understanding of the reproductive toxicity response of male marine invertebrates to POPs stress. [Display omitted] •First identification of epigenotoxic effects of PAHs on bivalve testis•PAHs caused marked decline in sex hormone synthesis and content in male clams.•PAHs inhibited DNA damage repair and cellular autophagy-apoptosis in clams' testis.•The toxic mechanism of PAHs on testis development of bivalves was first defined.•PAHs has distinct reproductive toxic effects on male clams.