Impact of polystyrene nanoplastics on apoptosis and inflammation in zebrafish larvae: Insights from reactive oxygen species perspective

In recent years, there has been a growing focus on the toxicity and mortality induced by nanoplastics (NPs) in aquatic organisms. However, studies investigating mechanisms underlying oxidative stress (OS), apoptosis, and inflammation induced by NPs in fish remain limited. This study observed that po...

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Veröffentlicht in:The Science of the total environment 2024-10, Vol.948, p.174737, Article 174737
Hauptverfasser: Pei, Jincheng, Chen, Shannan, Li, Li, Wang, Kailun, Pang, Anning, Niu, Mengmeng, Peng, Xueyun, Li, Nan, Wu, Hongjuan, Nie, Pin
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container_title The Science of the total environment
container_volume 948
creator Pei, Jincheng
Chen, Shannan
Li, Li
Wang, Kailun
Pang, Anning
Niu, Mengmeng
Peng, Xueyun
Li, Nan
Wu, Hongjuan
Nie, Pin
description In recent years, there has been a growing focus on the toxicity and mortality induced by nanoplastics (NPs) in aquatic organisms. However, studies investigating mechanisms underlying oxidative stress (OS), apoptosis, and inflammation induced by NPs in fish remain limited. This study observed that polystyrene NPs (PS-NPs) were accumulated into zebrafish larvae and zebrafish embryonic fibroblast (ZF4 cells), accompanied by the occurrence of pathological damage both at the cellular and tissue–organ level. Additionally, the transcriptional up-regulation of NADPH oxidases (NOXs) and subsequent excessive generation of reactive oxygen species (ROS) resulted in notable changes in the relative mRNA and protein expression levels associated with antioxidant oxidase systems in larvae. Furthermore, the study identified the impact of NPs on mitochondrial ultrastructural, resulting in mitochondrial depolarization and downregulation of mRNA expression related to the electron transport chain due to excessive ROS generation. Short-term exposure to NPs also triggered apoptosis and inflammation in zebrafish larvae, evident from significant up-regulation in mRNA expressions of proapoptotic factors and NF-κB proinflammatory signaling pathway, as well as increased transcription and protein levels of pro-inflammatory factors in larvae. Inhibition of intracellular excessive ROS effectively reduced the induction of apoptosis, NF-κB P65 nuclear migration levels, and cytokine secretion, underscoring OS as a pivotal factor throughout the process of apoptosis and inflammatory responses induced by NPs. This research significantly advances our comprehension of biological effects and underlying mechanisms of NPs in freshwater fish. [Display omitted] •PS-NPs translocate into ZF4 cells and cause excessive ROS.•PS-NPs cause oxidative stress and mitochondria dysfunction in larvae.•PS-NPs induce mitochondria-dependent apoptosis by triggering ROS.•PS-NPs induce inflammation through the ROS-driven NF-κB signaling pathway.
doi_str_mv 10.1016/j.scitotenv.2024.174737
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However, studies investigating mechanisms underlying oxidative stress (OS), apoptosis, and inflammation induced by NPs in fish remain limited. This study observed that polystyrene NPs (PS-NPs) were accumulated into zebrafish larvae and zebrafish embryonic fibroblast (ZF4 cells), accompanied by the occurrence of pathological damage both at the cellular and tissue–organ level. Additionally, the transcriptional up-regulation of NADPH oxidases (NOXs) and subsequent excessive generation of reactive oxygen species (ROS) resulted in notable changes in the relative mRNA and protein expression levels associated with antioxidant oxidase systems in larvae. Furthermore, the study identified the impact of NPs on mitochondrial ultrastructural, resulting in mitochondrial depolarization and downregulation of mRNA expression related to the electron transport chain due to excessive ROS generation. Short-term exposure to NPs also triggered apoptosis and inflammation in zebrafish larvae, evident from significant up-regulation in mRNA expressions of proapoptotic factors and NF-κB proinflammatory signaling pathway, as well as increased transcription and protein levels of pro-inflammatory factors in larvae. Inhibition of intracellular excessive ROS effectively reduced the induction of apoptosis, NF-κB P65 nuclear migration levels, and cytokine secretion, underscoring OS as a pivotal factor throughout the process of apoptosis and inflammatory responses induced by NPs. This research significantly advances our comprehension of biological effects and underlying mechanisms of NPs in freshwater fish. [Display omitted] •PS-NPs translocate into ZF4 cells and cause excessive ROS.•PS-NPs cause oxidative stress and mitochondria dysfunction in larvae.•PS-NPs induce mitochondria-dependent apoptosis by triggering ROS.•PS-NPs induce inflammation through the ROS-driven NF-κB signaling pathway.</description><identifier>ISSN: 0048-9697</identifier><identifier>ISSN: 1879-1026</identifier><identifier>EISSN: 1879-1026</identifier><identifier>DOI: 10.1016/j.scitotenv.2024.174737</identifier><identifier>PMID: 39004365</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>acute exposure ; Apoptosis ; cytokines ; Danio rerio ; electron transport chain ; environment ; fibroblasts ; freshwater fish ; gene expression ; Inflammation ; mitochondria ; mortality ; Nanoplastics ; oxidative stress ; oxidoreductases ; polystyrenes ; protein synthesis ; reactive oxygen species ; ROS ; secretion ; toxicity ; transcription (genetics)</subject><ispartof>The Science of the total environment, 2024-10, Vol.948, p.174737, Article 174737</ispartof><rights>2024 Elsevier B.V.</rights><rights>Copyright © 2024 Elsevier B.V. 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However, studies investigating mechanisms underlying oxidative stress (OS), apoptosis, and inflammation induced by NPs in fish remain limited. This study observed that polystyrene NPs (PS-NPs) were accumulated into zebrafish larvae and zebrafish embryonic fibroblast (ZF4 cells), accompanied by the occurrence of pathological damage both at the cellular and tissue–organ level. Additionally, the transcriptional up-regulation of NADPH oxidases (NOXs) and subsequent excessive generation of reactive oxygen species (ROS) resulted in notable changes in the relative mRNA and protein expression levels associated with antioxidant oxidase systems in larvae. Furthermore, the study identified the impact of NPs on mitochondrial ultrastructural, resulting in mitochondrial depolarization and downregulation of mRNA expression related to the electron transport chain due to excessive ROS generation. Short-term exposure to NPs also triggered apoptosis and inflammation in zebrafish larvae, evident from significant up-regulation in mRNA expressions of proapoptotic factors and NF-κB proinflammatory signaling pathway, as well as increased transcription and protein levels of pro-inflammatory factors in larvae. Inhibition of intracellular excessive ROS effectively reduced the induction of apoptosis, NF-κB P65 nuclear migration levels, and cytokine secretion, underscoring OS as a pivotal factor throughout the process of apoptosis and inflammatory responses induced by NPs. This research significantly advances our comprehension of biological effects and underlying mechanisms of NPs in freshwater fish. 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However, studies investigating mechanisms underlying oxidative stress (OS), apoptosis, and inflammation induced by NPs in fish remain limited. This study observed that polystyrene NPs (PS-NPs) were accumulated into zebrafish larvae and zebrafish embryonic fibroblast (ZF4 cells), accompanied by the occurrence of pathological damage both at the cellular and tissue–organ level. Additionally, the transcriptional up-regulation of NADPH oxidases (NOXs) and subsequent excessive generation of reactive oxygen species (ROS) resulted in notable changes in the relative mRNA and protein expression levels associated with antioxidant oxidase systems in larvae. Furthermore, the study identified the impact of NPs on mitochondrial ultrastructural, resulting in mitochondrial depolarization and downregulation of mRNA expression related to the electron transport chain due to excessive ROS generation. 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[Display omitted] •PS-NPs translocate into ZF4 cells and cause excessive ROS.•PS-NPs cause oxidative stress and mitochondria dysfunction in larvae.•PS-NPs induce mitochondria-dependent apoptosis by triggering ROS.•PS-NPs induce inflammation through the ROS-driven NF-κB signaling pathway.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>39004365</pmid><doi>10.1016/j.scitotenv.2024.174737</doi></addata></record>
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subjects acute exposure
Apoptosis
cytokines
Danio rerio
electron transport chain
environment
fibroblasts
freshwater fish
gene expression
Inflammation
mitochondria
mortality
Nanoplastics
oxidative stress
oxidoreductases
polystyrenes
protein synthesis
reactive oxygen species
ROS
secretion
toxicity
transcription (genetics)
title Impact of polystyrene nanoplastics on apoptosis and inflammation in zebrafish larvae: Insights from reactive oxygen species perspective
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