Internalized polystyrene nanoplastics trigger testicular damage and promote ferroptosis via CISD1 downregulation in mouse spermatocyte

Abstract Background There is a growing body of research regarding the potential reproductive toxicity of microplastics and nanoplastics. However, the underlying mechanisms by which nanoplastics exposure adversely affects the testes remain poorly understood. Our study aims to clarify the relationship...

Full description

Saved in:
Bibliographic Details
Main Authors: Jing Lv, Guangyu Liu, Ziqi Wang, Jueshun Zhang, Yuanyou Li, Yifan Wang, Ning Liu, Shayakhmetova Altyn, Zhongliang Jiang
Format: Article
Language:English
Published: BMC 2025-07-01
Series:Journal of Nanobiotechnology
Subjects:
Online Access:https://doi.org/10.1186/s12951-025-03620-7
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849235065265979392
author Jing Lv
Guangyu Liu
Ziqi Wang
Jueshun Zhang
Yuanyou Li
Yifan Wang
Ning Liu
Shayakhmetova Altyn
Zhongliang Jiang
author_facet Jing Lv
Guangyu Liu
Ziqi Wang
Jueshun Zhang
Yuanyou Li
Yifan Wang
Ning Liu
Shayakhmetova Altyn
Zhongliang Jiang
author_sort Jing Lv
collection DOAJ
description Abstract Background There is a growing body of research regarding the potential reproductive toxicity of microplastics and nanoplastics. However, the underlying mechanisms by which nanoplastics exposure adversely affects the testes remain poorly understood. Our study aims to clarify the relationship between ferritinophagy and mitochondrial dysfunction based on polystyrene nanoplastics (PS-NPs)-caused testicular damage in mice. Results The current study demonstrates that 50 nm PS-NPs accumulate in mouse testes and lead to a decrease in sperm quality and disruption of spermatocyte. Furthermore, PS-NPs trigger ferroptosis in GC-2 cells, which can be mitigated by deferiprone and 3-methyladenine. Further investigation reveals that PS-NPs initially aggregate in lysosomes and subsequently transfer to the mitochondria. This process increases mitochondrial Fe2+ and mitochondrial ROS levels, as well as reduces the expression of CISD1, a protein that inhibits the uptake and transport of Fe2+ into the mitochondrial matrix. These changes ultimately result in disturbances to mitochondrial structure and function. In terms of mechanism, pioglitazone, a drug that stabilizes CISD1, has been demonstrated to mitigate ferroptosis induced by NCOA4-mediated ferritinophagy in GC-2 cells. Conclusions Our results indicate that PS-NPs cause mouse testicular damage through ferroptosis. Mechanistically, we confirmed that PS-NPs trigger NCOA4-mediated ferritinophagy and CISD1 downregulation in spermatocyte, which aggravates the flow of ferrous iron from the cytoplasm to the mitochondria.
format Article
id doaj-art-3819cd08dc1f4e088eb305347a782f3e
institution Kabale University
issn 1477-3155
language English
publishDate 2025-07-01
publisher BMC
record_format Article
series Journal of Nanobiotechnology
spelling doaj-art-3819cd08dc1f4e088eb305347a782f3e2025-08-20T04:02:55ZengBMCJournal of Nanobiotechnology1477-31552025-07-0123112010.1186/s12951-025-03620-7Internalized polystyrene nanoplastics trigger testicular damage and promote ferroptosis via CISD1 downregulation in mouse spermatocyteJing Lv0Guangyu Liu1Ziqi Wang2Jueshun Zhang3Yuanyou Li4Yifan Wang5Ning Liu6Shayakhmetova Altyn7Zhongliang Jiang8Key Laboratory of Animal Genetic, Breeding and Reproduction in Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetic, Breeding and Reproduction in Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetic, Breeding and Reproduction in Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetic, Breeding and Reproduction in Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Bio-Resources and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan UniversityKey Laboratory of Animal Genetic, Breeding and Reproduction in Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetic, Breeding and Reproduction in Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityAgrotechnological Faculty, M.Kozybayev North Kazakhstan UniversityKey Laboratory of Animal Genetic, Breeding and Reproduction in Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityAbstract Background There is a growing body of research regarding the potential reproductive toxicity of microplastics and nanoplastics. However, the underlying mechanisms by which nanoplastics exposure adversely affects the testes remain poorly understood. Our study aims to clarify the relationship between ferritinophagy and mitochondrial dysfunction based on polystyrene nanoplastics (PS-NPs)-caused testicular damage in mice. Results The current study demonstrates that 50 nm PS-NPs accumulate in mouse testes and lead to a decrease in sperm quality and disruption of spermatocyte. Furthermore, PS-NPs trigger ferroptosis in GC-2 cells, which can be mitigated by deferiprone and 3-methyladenine. Further investigation reveals that PS-NPs initially aggregate in lysosomes and subsequently transfer to the mitochondria. This process increases mitochondrial Fe2+ and mitochondrial ROS levels, as well as reduces the expression of CISD1, a protein that inhibits the uptake and transport of Fe2+ into the mitochondrial matrix. These changes ultimately result in disturbances to mitochondrial structure and function. In terms of mechanism, pioglitazone, a drug that stabilizes CISD1, has been demonstrated to mitigate ferroptosis induced by NCOA4-mediated ferritinophagy in GC-2 cells. Conclusions Our results indicate that PS-NPs cause mouse testicular damage through ferroptosis. Mechanistically, we confirmed that PS-NPs trigger NCOA4-mediated ferritinophagy and CISD1 downregulation in spermatocyte, which aggravates the flow of ferrous iron from the cytoplasm to the mitochondria.https://doi.org/10.1186/s12951-025-03620-7Polystyrene nanoplasticsTestesSpermatocyteFerritinophagyCISD1
spellingShingle Jing Lv
Guangyu Liu
Ziqi Wang
Jueshun Zhang
Yuanyou Li
Yifan Wang
Ning Liu
Shayakhmetova Altyn
Zhongliang Jiang
Internalized polystyrene nanoplastics trigger testicular damage and promote ferroptosis via CISD1 downregulation in mouse spermatocyte
Journal of Nanobiotechnology
Polystyrene nanoplastics
Testes
Spermatocyte
Ferritinophagy
CISD1
title Internalized polystyrene nanoplastics trigger testicular damage and promote ferroptosis via CISD1 downregulation in mouse spermatocyte
title_full Internalized polystyrene nanoplastics trigger testicular damage and promote ferroptosis via CISD1 downregulation in mouse spermatocyte
title_fullStr Internalized polystyrene nanoplastics trigger testicular damage and promote ferroptosis via CISD1 downregulation in mouse spermatocyte
title_full_unstemmed Internalized polystyrene nanoplastics trigger testicular damage and promote ferroptosis via CISD1 downregulation in mouse spermatocyte
title_short Internalized polystyrene nanoplastics trigger testicular damage and promote ferroptosis via CISD1 downregulation in mouse spermatocyte
title_sort internalized polystyrene nanoplastics trigger testicular damage and promote ferroptosis via cisd1 downregulation in mouse spermatocyte
topic Polystyrene nanoplastics
Testes
Spermatocyte
Ferritinophagy
CISD1
url https://doi.org/10.1186/s12951-025-03620-7
work_keys_str_mv AT jinglv internalizedpolystyrenenanoplasticstriggertesticulardamageandpromoteferroptosisviacisd1downregulationinmousespermatocyte
AT guangyuliu internalizedpolystyrenenanoplasticstriggertesticulardamageandpromoteferroptosisviacisd1downregulationinmousespermatocyte
AT ziqiwang internalizedpolystyrenenanoplasticstriggertesticulardamageandpromoteferroptosisviacisd1downregulationinmousespermatocyte
AT jueshunzhang internalizedpolystyrenenanoplasticstriggertesticulardamageandpromoteferroptosisviacisd1downregulationinmousespermatocyte
AT yuanyouli internalizedpolystyrenenanoplasticstriggertesticulardamageandpromoteferroptosisviacisd1downregulationinmousespermatocyte
AT yifanwang internalizedpolystyrenenanoplasticstriggertesticulardamageandpromoteferroptosisviacisd1downregulationinmousespermatocyte
AT ningliu internalizedpolystyrenenanoplasticstriggertesticulardamageandpromoteferroptosisviacisd1downregulationinmousespermatocyte
AT shayakhmetovaaltyn internalizedpolystyrenenanoplasticstriggertesticulardamageandpromoteferroptosisviacisd1downregulationinmousespermatocyte
AT zhongliangjiang internalizedpolystyrenenanoplasticstriggertesticulardamageandpromoteferroptosisviacisd1downregulationinmousespermatocyte