Polystyrene microplastics induced spermatogenesis disorder via disrupting mitochondrial function through the regulation of the Sirt1-Pgc1α signaling pathway in male mice

Haibo Jin; Bowen Xue; Xuefang Chen; Tan Ma; Yonggang Ma; Hui Zou; Jiaqiao Zhu; Xishuai Tong; Ruilong Song; Weiqian Meng; Zongping Liu

doi:10.1016/j.envpol.2024.125364

Polystyrene microplastics induced spermatogenesis disorder via disrupting mitochondrial function through the regulation of the Sirt1-Pgc1α signaling pathway in male mice

Environ Pollut. 2025 Jan 1;364(Pt 2):125364. doi: 10.1016/j.envpol.2024.125364. Epub 2024 Nov 23.

Authors

Haibo Jin¹, Bowen Xue², Xuefang Chen³, Tan Ma⁴, Yonggang Ma⁵, Hui Zou⁶, Jiaqiao Zhu⁷, Xishuai Tong⁸, Ruilong Song⁹, Weiqian Meng¹⁰, Zongping Liu¹¹

Affiliations

¹ School of Public Health, Yangzhou University, Yangzhou, Jiangsu, 225000, China; College of Veterinary Medicine, Yangzhou University, Yangzhou, 225009, China; Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China; Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, 225009, China. Electronic address: [email protected].
² College of Veterinary Medicine, Yangzhou University, Yangzhou, 225009, China; Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China; Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, 225009, China. Electronic address: [email protected].
³ School of Public Health, Yangzhou University, Yangzhou, Jiangsu, 225000, China; College of Veterinary Medicine, Yangzhou University, Yangzhou, 225009, China; Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China; Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, 225009, China. Electronic address: [email protected].
⁴ Institute of Translational Medicine, Medical College, Yangzhou University, Yangzhou, 225001, Jiangsu, China; Jiangsu Key Laboratory of Integrated Traditional Chinese and Western Medicine for Prevention and Treatment of Senile Disease, Yangzhou University, Yangzhou, 225001, Jiangsu, China. Electronic address: [email protected].
⁵ College of Veterinary Medicine, Yangzhou University, Yangzhou, 225009, China; Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China; Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, 225009, China. Electronic address: [email protected].
⁶ College of Veterinary Medicine, Yangzhou University, Yangzhou, 225009, China; Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China; Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, 225009, China. Electronic address: [email protected].
⁷ College of Veterinary Medicine, Yangzhou University, Yangzhou, 225009, China; Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China; Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, 225009, China. Electronic address: [email protected].
⁸ College of Veterinary Medicine, Yangzhou University, Yangzhou, 225009, China; Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China; Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, 225009, China. Electronic address: [email protected].
⁹ College of Veterinary Medicine, Yangzhou University, Yangzhou, 225009, China; Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China; Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, 225009, China. Electronic address: [email protected].
¹⁰ College of Health Science, Rush University, Chicago, IL, 60612, USA. Electronic address: [email protected].
¹¹ School of Public Health, Yangzhou University, Yangzhou, Jiangsu, 225000, China; College of Veterinary Medicine, Yangzhou University, Yangzhou, 225009, China; Joint International Research Laboratory of Agriculture and Agri-Product Safety, Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China; Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, 225009, China. Electronic address: [email protected].

PMID: 39577614
DOI: 10.1016/j.envpol.2024.125364

Abstract

Microplastics (MPs) have emerged as hazardous substances, eliciting widespread concern regarding their potential toxicity. Although our previous research has indicated that polystyrene MPs (PS-MPs) might cause male reproductive toxicity in mammals, their precise effects on sperm motility parameters and acrosomal development remain uncertain. Herein, the effects on sperm motility of PS-MPs at varied particle sizes (0.5 μm, 4 μm and 10 μm) and the underlying mechanisms were examined. The results revealed that PS-MPs caused a decrease in sperm motility, accompanied by abnormalities in the structure and function of the sperm acrosome. Meanwhile, PS-MPs triggered the elevation of intracellular reactive oxygen species levels and the abnormal expression of antioxidant enzymes (γH2AX, GPX4, Peroxiredoxin 5 and SDHB), indicating disruption of the sperm antioxidant system. Furthermore, we observed aberrant expression of key factors involved in mitochondrial fission/fusion (Drp1, Fis1, Mfn1, Mfn2) and biogenesis (Tfam, Nrf1, Pgc1α), potentially resulting in disrupted mitochondrial dynamics and biogenesis in mice testis and Sertoli cells exposed to PS-MPs. Additionally, PS-MPs induced mitochondrial dysfunction by regulating the Sirt1-Pgc1α signaling pathway. Our data provided novel insights into potential mechanisms underlying the spermatogenesis disorders triggered by PS-MPs.

Keywords: Mitochondrial biogenesis; Mitochondrial dynamics; PS-MPs; Sperm motility; Spermatogenesis disorder.

MeSH terms

Animals
Male
Mice
Microplastics* / toxicity
Mitochondria* / drug effects
Mitochondria* / metabolism
Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha* / genetics
Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha* / metabolism
Polystyrenes* / toxicity
Reactive Oxygen Species / metabolism
Signal Transduction* / drug effects
Sirtuin 1* / genetics
Sirtuin 1* / metabolism
Sperm Motility / drug effects
Spermatogenesis* / drug effects
Spermatozoa / drug effects
Testis / drug effects
Testis / metabolism

Substances

Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
Sirtuin 1
Microplastics
Polystyrenes
Ppargc1a protein, mouse
Sirt1 protein, mouse
Reactive Oxygen Species