Size-dependent deleterious effects of nano- and microplastics on sperm motility

Ziyi Lin; Zijie Li; Shuqin Ji; Hoi Shing Lo; Baki Billah; Ayesha Sharmin; Xiaofang Han; Wing-Yee Lui; William Ka Fai Tse; James Kar-Hei Fang; Chunqiu Zhang; Xuejun Shang; Keng Po Lai; Lei Li

doi:10.1016/j.tox.2024.153834

Size-dependent deleterious effects of nano- and microplastics on sperm motility

Toxicology. 2024 Aug:506:153834. doi: 10.1016/j.tox.2024.153834. Epub 2024 May 18.

Authors

Ziyi Lin¹, Zijie Li², Shuqin Ji², Hoi Shing Lo³, Baki Billah⁴, Ayesha Sharmin⁵, Xiaofang Han⁶, Wing-Yee Lui⁷, William Ka Fai Tse⁸, James Kar-Hei Fang⁹, Chunqiu Zhang¹⁰, Xuejun Shang¹¹, Keng Po Lai¹², Lei Li¹³

Affiliations

¹ The Brain Cognition and Brain Disease Institute, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China; University of Chinese Academy of Sciences, Beijing, China.
² The Brain Cognition and Brain Disease Institute, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China.
³ Department of Environmental Science, Stockholm University, Stockholm, Sweden.
⁴ Department of Zoology, Jahangirnagar University, Savar, Dhaka, Bangladesh.
⁵ Department of Chemistry, Bangladesh University of Engineering and Technology, Dhaka, Bangladesh.
⁶ Core Laboratory, Shanxi Provincial People's Hospital (Fifth Hospital) of Shanxi Medical University, Taiyuan, China.
⁷ School of Biological Sciences, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region of China.
⁸ Laboratory of Developmental Disorders and Toxicology, Center for Promotion of International Education and Research, Faculty of Agriculture, Kyushu University, Fukuoka, Japan.
⁹ Department of Food Science and Nutrition, The Hong Kong Polytechnic University, Hung Hom, Hong Kong Special Administrative Region of China; State Key Laboratory of Marine Pollution, City University of Hong Kong, Kowloon Tong, Hong Kong Special Administrative Region of China.
¹⁰ Key Laboratory of Biomedical Imaging Science and System, Chinese Academy of Sciences, Shenzhen, China.
¹¹ Department of Urology, Jinling Hospital, School of Medicine, Nanjing University, Nanjing, China. Electronic address: shangxj98@163.com.
¹² Key Laboratory of Environmental Pollution and Integrative Omics, Guilin Medical University, Education Department of Guangxi Zhuang Autonomous Region, China. Electronic address: kengplai@cityu.edu.hk.
¹³ The Brain Cognition and Brain Disease Institute, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China; University of Chinese Academy of Sciences, Beijing, China; Guangdong Provincial Key Laboratory of Brain Connectome and Behavior, CAS Key Laboratory of Brain Connectome and Manipulation, Shenzhen, China; Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions, Shenzhen, China. Electronic address: saralilei@siat.ac.cn.

PMID: 38763425
DOI: 10.1016/j.tox.2024.153834

Abstract

Introduction: Growing concerns regarding the reproductive toxicity associated with daily life exposure to micro-/nano-plastics (abbreviated as MNPs) have become increasingly prevalent. In reality, MNPs exposure involves a heterogeneous mixture of MNPs of different sizes rather than a single size.

Methods: In this study, an oral exposure mouse model was used to evaluate the effects of MNPs of four size ranges: 25-30 nm, 1-5 µm, 20-27 µm, and 125-150 µm. Adult male C57BL/6 J mice were administered environmentally relevant concentrations of 0.1 mg MNPs/day for 21 days. After that, open field test and computer assisted sperm assessment (CASA) were conducted. Immunohistochemical analyses of organ and cell type localization of MNPs were evaluated. Testicular transcriptome analysis was carried out to understand the molecular mechanisms.

Results: Our result showed that MNPs of different size ranges all impaired sperm motility, with a decrease in progressive sperm motility, linearity and straight-line velocity of sperm movement. Alterations did not manifest in animal locomotion, body weight, or sperm count. Noteworthy effects were most pronounced in the smaller MNPs size ranges (25-30 nm and 1-5 µm). Linear regression analysis substantiated a negative correlation between the size of MNPs and sperm curvilinear activity. Immunohistochemical analysis unveiled the intrusions of 1-5 µm MNPs, but not 20-27 µm and 125-150 µm MNPs, into Leydig cells and testicular macrophages. Further testicular transcriptomic analysis revealed perturbations in pathways related to spermatogenesis, oxidative stress, and inflammation. Particularly within the 1-5 µm MNPs group, a heightened perturbation in pathways linked to spermatogenesis and oxidative stress was observed.

Conclusions: Our data support the size-dependent impairment of MNPs on sperm functionality, underscoring the pressing need for apprehensions about and interventions against the escalation of environmental micro-/nano-plastics contamination. This urgency is especially pertinent to small-sized MNPs.

Keywords: Micro-/nano-plastics; Reproductive toxicity; Size-dependent; Sperm quality; Testicular macrophage.

MeSH terms

Animals
Male
Mice
Mice, Inbred C57BL*
Microplastics* / toxicity
Nanoparticles / toxicity
Oxidative Stress / drug effects
Particle Size*
Sperm Motility* / drug effects
Spermatozoa / drug effects
Testis* / drug effects
Testis* / metabolism
Testis* / pathology

Substances

Microplastics