Polyethylene microplastic exposure adversely affects oocyte quality in human and mouse

Qiaoling Wang; Fengli Chi; Yingdong Liu; Qiurong Chang; Siyu Chen; Pengcheng Kong; Wanli Yang; Wenqiang Liu; Xiaoming Teng; Yan Zhao; Yi Guo

doi:10.1016/j.envint.2024.109236

Polyethylene microplastic exposure adversely affects oocyte quality in human and mouse

Environ Int. 2024 Dec 25:195:109236. doi: 10.1016/j.envint.2024.109236. Online ahead of print.

Authors

Qiaoling Wang¹, Fengli Chi¹, Yingdong Liu², Qiurong Chang¹, Siyu Chen¹, Pengcheng Kong¹, Wanli Yang¹, Wenqiang Liu¹, Xiaoming Teng³, Yan Zhao⁴, Yi Guo⁵

Affiliations

¹ Center for Reproductive Medicine, Shanghai First Maternity and Infant Hospital, School of Medicine, Tongji University, Shanghai, China.
² Shanghai Key Laboratory of Signaling and Disease Research, Frontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji University, Shanghai, China.
³ Center for Reproductive Medicine, Shanghai First Maternity and Infant Hospital, School of Medicine, Tongji University, Shanghai, China. Electronic address: Tengxiaomign@51mch.com.
⁴ Hospital of Obstetrics and Gynecology, Shanghai Medical School, Fudan University, Shanghai, China. Electronic address: zy861201@163.com.
⁵ Center for Reproductive Medicine, Shanghai First Maternity and Infant Hospital, School of Medicine, Tongji University, Shanghai, China. Electronic address: gy_guoyi@tongji.edu.cn.

PMID: 39729868
DOI: 10.1016/j.envint.2024.109236

Abstract

Microplastics (MPs) are pervasive environmental contaminants, resulting in unavoidable human exposure. This study identified MPs in follicular fluid and investigated the specific MPs and mechanisms that adversely affect oocytes. MPs in the follicular fluid of 44 infertile women undergoing assisted reproductive technology were measured using Raman microspectroscopy. Differential metabolites in follicular fluid were analyzed via untargeted metabolomics. Female mice were exposed to polyethylene (PE) to validate human findings. MPs, particularly PE, exhibited the highest detection rate (86.4 %) in human follicular fluid and showed a negative correlation with fertilization rates (r = -0.407, P = 0.007). Elevated PE levels altered metabolites primarily involved in metabolic pathways, ferroptosis, and ovarian steroidogenesis. In mice, PE exposure significantly reduced the number of retrieved oocytes (31.5 vs. 36.3, P < 0.05) and fertilization rate (70.8 % vs. 85.2 %, P < 0.001), while increasing the proportion of poor-quality oocytes (28.2 % vs. 16.5 %, P < 0.001) and reactive oxygen species (ROS) production compared to controls. RNA sequencing indicated significant upregulation of inflammation-related genes (Il10ra, Il1a, Il33, Tnfaip8l2, and Tnfrsf1b) in the PE-exposed group. In conclusion, PE exposure impairs oocyte quality possibly by disrupting follicular fluid metabolism, elevating inflammation-related gene expression, and increasing ROS production in oocytes.

Keywords: Follicular fluid; Microplastics; Oocytes; Polyethylene.