Ferroptosis: First evidence in premature duck ovary induced by polyvinyl chloride microplastics

Waseem Ali; Yan Chen; Muhammad Ghiasuddin Shah; Rehana Shahnawaz Buriro; Jian Sun; Zongping Liu; Hui Zou

doi:10.1016/j.scitotenv.2024.173032

Ferroptosis: First evidence in premature duck ovary induced by polyvinyl chloride microplastics

Sci Total Environ. 2024 May 9:933:173032. doi: 10.1016/j.scitotenv.2024.173032. Online ahead of print.

Authors

Waseem Ali¹, Yan Chen¹, Muhammad Ghiasuddin Shah¹, Rehana Shahnawaz Buriro¹, Jian Sun¹, Zongping Liu², Hui Zou³

Affiliations

¹ College of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu 225009, China; Joint International Research Laboratory of Agriculture and Agri-Product Safety of the Ministry of Education of China, Yangzhou University, Yangzhou, Jiangsu 225009, China; Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, Jiangsu 225009, China.
² College of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu 225009, China; Joint International Research Laboratory of Agriculture and Agri-Product Safety of the Ministry of Education of China, Yangzhou University, Yangzhou, Jiangsu 225009, China; Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, Jiangsu 225009, China. Electronic address: liuzongping@yzu.edu.cn.
³ College of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu 225009, China; Joint International Research Laboratory of Agriculture and Agri-Product Safety of the Ministry of Education of China, Yangzhou University, Yangzhou, Jiangsu 225009, China; Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, Jiangsu 225009, China. Electronic address: zouhui@yzu.edu.cn.

PMID: 38734099
DOI: 10.1016/j.scitotenv.2024.173032

Abstract

Ferroptosis is frequently observed in fibrosis and diseases related to iron metabolism disorders in various mammalian organs. However, research regarding the damage mechanism of ferroptosis in the female reproductive system of avian species remains unclear. In this study, Muscovy female ducks were divided into three groups which were given purified water, 1 mg/L polyvinyl chloride microplastics (PVC-MPs) and 10 mg/L PVC-MPs for two months respectively, to investigate the ferroptosis induced by PVC-MPs caused ovarian tissue fibrosis that lead to premature ovarian failure. The results showed that the high accumulation of PVC-MPs in ovarian tissue affected the morphology and functional activity of ovarian granulosa cells (GCs) and subsequently caused the follicular development disorders and down-regulated the immunosignaling of ovarian steroidogenesis proteins 3β-hydroxysteroid dehydrogenase (3β-HSD), 17β-hydroxysteroid dehydrogenase (17β-HSD), CYP11A1 cytochrome (P450-11A1) and CYP17A1 cytochrome (P450-17A1) suggested impaired ovarian function. In addition, PVC-MPs significantly up-regulated positive expression of collagen fibers, significantly increased lipid peroxidation and malondialdehyde (MDA) level, along with encouraged overload of iron contents in the ovarian tissue were the characteristics of ferroptosis. Further, immunohistochemistry results confirmed that immunosignaling of ferroptosis related proteins Acyl-CoA synthetase (ACSL4), Cyclooxygenase 2 (COX2) and ferritin heavy chain 1 (FTH1) were significantly increased, but solute carrier family 7 member 11 (SLC7A11) and glutathione peroxidase (GPX4) were decreased by PVC-MPs in the ovarian tissue. In conclusion, our study demonstrates that PVC-MPs induced ferroptosis in the ovarian GCs, leading to follicle development disorders and ovarian tissue fibrosis, and ultimately contributing to various female reproductive disorders through regulating the proteins expression of ferroptosis.

Keywords: Duck; Ferroptosis; Iron contents; Ovarian tissue fibrosis; PVC-MPs.