Ototoxicity of polystyrene nanoplastics in mice, HEI-OC1 cells and zebrafish

Polystyrene nanoplastics are a novel class of pollutants. They are easily absorbed by living organisms, and their potential toxicity has raised concerns. However, the impact of polystyrene nanoplastics on auditory organs remains unknown. Here, our results showed that polystyrene nanoplastics entered...

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Main Authors: Yuancheng Wu, Lianzhen Li, Lihuan Tang, Willie Peijnenburg, Huangruici Zhang, Daoli Xie, Ruishuang Geng, Tihua Zheng, Liyan Bi, Xiaodan Wei, Han-jung Chae, Lan Wang, Li Zhao, Bo Li, Qingyin Zheng
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-02-01
Series:Frontiers in Molecular Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnmol.2024.1345536/full
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author Yuancheng Wu
Lianzhen Li
Lihuan Tang
Willie Peijnenburg
Willie Peijnenburg
Huangruici Zhang
Daoli Xie
Ruishuang Geng
Tihua Zheng
Liyan Bi
Xiaodan Wei
Han-jung Chae
Lan Wang
Li Zhao
Bo Li
Qingyin Zheng
author_facet Yuancheng Wu
Lianzhen Li
Lihuan Tang
Willie Peijnenburg
Willie Peijnenburg
Huangruici Zhang
Daoli Xie
Ruishuang Geng
Tihua Zheng
Liyan Bi
Xiaodan Wei
Han-jung Chae
Lan Wang
Li Zhao
Bo Li
Qingyin Zheng
author_sort Yuancheng Wu
collection DOAJ
description Polystyrene nanoplastics are a novel class of pollutants. They are easily absorbed by living organisms, and their potential toxicity has raised concerns. However, the impact of polystyrene nanoplastics on auditory organs remains unknown. Here, our results showed that polystyrene nanoplastics entered the cochlea of mice, HEI-OC1 cells, and lateral line hair cells of zebrafish, causing cellular injury and increasing apoptosis. Additionally, we found that exposure to polystyrene nanoplastics resulted in a significant elevation in the auditory brainstem response thresholds, a loss of auditory sensory hair cells, stereocilia degeneration and a decrease in expression of Claudin-5 and Occludin proteins at the blood-lymphatic barrier in mice. We also observed a significant decrease in the acoustic alarm response of zebrafish after exposure to polystyrene nanoplastics. Mechanistic analysis revealed that polystyrene nanoplastics induced up-regulation of the Nrf2/HO-1 pathway, increased levels of malondialdehyde, and decreased superoxide dismutase and catalase levels in cochlea and HEI-OC1 cells. Furthermore, we observed that the expression of ferroptosis-related indicators GPX4 and SLC7A11 decreased as well as increased expression of ACLS4 in cochlea and HEI-OC1 cells. This study also revealed that polystyrene nanoplastics exposure led to increased expression of the inflammatory factors TNF-α, IL-1β and COX2 in cochlea and HEI-OC1 cells. Further research found that the cell apoptosis, ferroptosis and inflammatory reactions induced by polystyrene nanoplastics in HEI-OC1 cells was reversed through the pretreatment with N-acetylcysteine, a reactive oxygen species inhibitor. Overall, our study first discovered and systematically revealed the ototoxicity of polystyrene nanoplastics and its underlying mechanism.
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spelling doaj.art-31e32b2870594c6ab5d9c8d49bca77f92024-02-19T04:23:16ZengFrontiers Media S.A.Frontiers in Molecular Neuroscience1662-50992024-02-011710.3389/fnmol.2024.13455361345536Ototoxicity of polystyrene nanoplastics in mice, HEI-OC1 cells and zebrafishYuancheng Wu0Lianzhen Li1Lihuan Tang2Willie Peijnenburg3Willie Peijnenburg4Huangruici Zhang5Daoli Xie6Ruishuang Geng7Tihua Zheng8Liyan Bi9Xiaodan Wei10Han-jung Chae11Lan Wang12Li Zhao13Bo Li14Qingyin Zheng15Hearing and Speech Rehabilitation Institute, Binzhou Medical University, Yantai, ChinaCollege of Environmental Sciences and Engineering, Qingdao University, Qingdao, ChinaHearing and Speech Rehabilitation Institute, Binzhou Medical University, Yantai, ChinaInstitute of Environmental Sciences (CML), Leiden University, Leiden, NetherlandsNational Institute of Public Health and the Environment (RIVM), Center for Safety of Substances and Products, Bilthoven, NetherlandsHearing and Speech Rehabilitation Institute, Binzhou Medical University, Yantai, ChinaHearing and Speech Rehabilitation Institute, Binzhou Medical University, Yantai, ChinaHearing and Speech Rehabilitation Institute, Binzhou Medical University, Yantai, ChinaHearing and Speech Rehabilitation Institute, Binzhou Medical University, Yantai, ChinaHearing and Speech Rehabilitation Institute, Binzhou Medical University, Yantai, ChinaDepartment of Pathology, School of Basic Medicine, Binzhou Medical University, Yantai, ChinaSchool of Pharmacy, Jeonbuk National University, Jeonju, Republic of KoreaHearing and Speech Rehabilitation Institute, Binzhou Medical University, Yantai, ChinaHearing and Speech Rehabilitation Institute, Binzhou Medical University, Yantai, ChinaHearing and Speech Rehabilitation Institute, Binzhou Medical University, Yantai, ChinaDepartment of Otolaryngology-Head and Neck Surgery, Case Western Reserve University, Cleveland, OH, United StatesPolystyrene nanoplastics are a novel class of pollutants. They are easily absorbed by living organisms, and their potential toxicity has raised concerns. However, the impact of polystyrene nanoplastics on auditory organs remains unknown. Here, our results showed that polystyrene nanoplastics entered the cochlea of mice, HEI-OC1 cells, and lateral line hair cells of zebrafish, causing cellular injury and increasing apoptosis. Additionally, we found that exposure to polystyrene nanoplastics resulted in a significant elevation in the auditory brainstem response thresholds, a loss of auditory sensory hair cells, stereocilia degeneration and a decrease in expression of Claudin-5 and Occludin proteins at the blood-lymphatic barrier in mice. We also observed a significant decrease in the acoustic alarm response of zebrafish after exposure to polystyrene nanoplastics. Mechanistic analysis revealed that polystyrene nanoplastics induced up-regulation of the Nrf2/HO-1 pathway, increased levels of malondialdehyde, and decreased superoxide dismutase and catalase levels in cochlea and HEI-OC1 cells. Furthermore, we observed that the expression of ferroptosis-related indicators GPX4 and SLC7A11 decreased as well as increased expression of ACLS4 in cochlea and HEI-OC1 cells. This study also revealed that polystyrene nanoplastics exposure led to increased expression of the inflammatory factors TNF-α, IL-1β and COX2 in cochlea and HEI-OC1 cells. Further research found that the cell apoptosis, ferroptosis and inflammatory reactions induced by polystyrene nanoplastics in HEI-OC1 cells was reversed through the pretreatment with N-acetylcysteine, a reactive oxygen species inhibitor. Overall, our study first discovered and systematically revealed the ototoxicity of polystyrene nanoplastics and its underlying mechanism.https://www.frontiersin.org/articles/10.3389/fnmol.2024.1345536/fullpolystyrene nanoplasticsototoxicityhearing lossenvironmental ototoxicantsreactive oxygen speciesinflammation
spellingShingle Yuancheng Wu
Lianzhen Li
Lihuan Tang
Willie Peijnenburg
Willie Peijnenburg
Huangruici Zhang
Daoli Xie
Ruishuang Geng
Tihua Zheng
Liyan Bi
Xiaodan Wei
Han-jung Chae
Lan Wang
Li Zhao
Bo Li
Qingyin Zheng
Ototoxicity of polystyrene nanoplastics in mice, HEI-OC1 cells and zebrafish
Frontiers in Molecular Neuroscience
polystyrene nanoplastics
ototoxicity
hearing loss
environmental ototoxicants
reactive oxygen species
inflammation
title Ototoxicity of polystyrene nanoplastics in mice, HEI-OC1 cells and zebrafish
title_full Ototoxicity of polystyrene nanoplastics in mice, HEI-OC1 cells and zebrafish
title_fullStr Ototoxicity of polystyrene nanoplastics in mice, HEI-OC1 cells and zebrafish
title_full_unstemmed Ototoxicity of polystyrene nanoplastics in mice, HEI-OC1 cells and zebrafish
title_short Ototoxicity of polystyrene nanoplastics in mice, HEI-OC1 cells and zebrafish
title_sort ototoxicity of polystyrene nanoplastics in mice hei oc1 cells and zebrafish
topic polystyrene nanoplastics
ototoxicity
hearing loss
environmental ototoxicants
reactive oxygen species
inflammation
url https://www.frontiersin.org/articles/10.3389/fnmol.2024.1345536/full
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