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Male reproductive toxicity involved in spermatogenesis induced by perfluorooctane sulfonate and perfluorooctanoic acid in Caenorhabditis elegans

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Abstract

As a persistent organic pollutant, perfluorooctane sulfonate (PFOS) and perfluorooctanoic acid (PFOA) have gained increasing research attention over recent years because of their potential risk to humans and the environment. In this paper, we investigated the reproductive toxicity of these pollutants using a C. elegans model to evaluate spermatogenesis throughout the entire developmental cycle of him-5 mutant by exposing to 0.001, 0.01, and 0.1 mmol/L PFOS or PFOA for 48 h. Experimental results suggested that PFOS and PFOA exposure led to reductions in brood size, germ cell number, spermatid size, and motility, and increases in rate of malformation spermatids. Analysis of variance (ANOVA) showed that exposure to PFOS resulted in higher levels of damage than PFOA in germ cells only in 0.001 mmol/L exposure group. RT-qPCR was used to further investigate the expression of genes associated with different stages of spermatogenesis, such as mitosis and meiosis, fibrous body-membranous organelles (FB-MOs), and sperm activation. The expression levels of wee-1.3, spe-4, spe-6, and spe-17 genes were increased, while those of puf-8, spe-10, fer-1, swm-1, try-5, and spe-15 genes were decreased. Our results suggesting that PFOS or PFOA may cause spermatogenesis damage by disrupting the mitotic proliferation, meiotic entry, formation of the MOs, fusion of the MOs and plasma membrane (PM), and pseudopods. Loss-of-function studies using puf-8 and spe-10 mutants revealed spe-10 gene was specifically involved in PFOS- or PFOA-induced reproductive toxicity via regulating one or more critical palmitoylation events, while puf-8 gene was not direct target of PFOS and PFOA, and PFOS and PFOA may act on the upstream gene of puf-8, thus affecting reproductive ability. Taken together, these results demonstrate the potential adverse impact of PFOS and PFOA exposure on spermatogenesis and provide valuable data for PFC risk assessment.

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Abbreviations

PFCs:

Perfluorinated compounds

PFOS:

Perfluorooctane sulfonate

PFOA:

Perfluorooctanoic acid

FB-MOs:

Fibrous body-membranous organelles

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Funding

This work was financially supported by Major Science and Technology Program for Water Pollution Control and Treatment (2014ZX07405002), National Natural Science Foundation of China grants (81872579, 81273123), Graduate Student Scientific Practice Innovation Projects in Jiangsu Province (KYCX19_0123), and Fundamental Research Fund of Central Public Welfare Research Institutions in 2019 (Innovation team project of new approach and application on substitution toxicology of environmental hormone substance).

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Authors and Affiliations

  1. Key Laboratory of Environmental Medicine Engineering, Ministry of Education, School of Public Health, Southeast University, Nanjing, 210009, China

    Jiechen Yin, Zihai Jian, Xiaojin Yu, Yuepu Pu, Lihong Yin, Dayong Wang & Ran Liu

  2. Nanjing Institute of Environmental Science, Key Laboratory of Pesticide Environmental Assessment and Pollution Control, Ministry of Ecology and Environment, Nanjing, 210042, China

    Jiechen Yin & Yuanqing Bu

  3. Key Laboratory of Environmental Medicine Engineering, Ministry of Education, School of Energy and Environment, Southeast University, Nanjing, 210096, China

    Guangcan Zhu

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  1. Jiechen Yin
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Correspondence to Ran Liu.

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Yin, J., Jian, Z., Zhu, G. et al. Male reproductive toxicity involved in spermatogenesis induced by perfluorooctane sulfonate and perfluorooctanoic acid in Caenorhabditis elegans. Environ Sci Pollut Res 28, 1443–1453 (2021). https://doi.org/10.1007/s11356-020-10530-8

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