Quantum Dots‐caused Retinal Degeneration in Zebrafish Regulated by Ferroptosis and Mitophagy in Retinal Pigment Epithelial Cells through Inhibiting Spliceosome

Abstract Quantum dots (QDs) are widely used, but their health impact on the visual system is little known. This study aims to elucidate the effects and mechanisms of typical metallic QDs on retinas using zebrafish. Comprehensive histology, imaging, and bulk RNA sequencing reveal that InP/ZnS QDs cau...

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Main Authors: Naying Zheng, Tingting Liao, Chuchu Zhang, Zheyang Zhang, Sen Yan, Xiaohan Xi, Fengkai Ruan, Chunyan Yang, Qingliang Zhao, Wenbo Deng, Jialiang Huang, Zi‐Tao Huang, Zhi‐Feng Chen, Xiang Wang, Qingming Qu, Zhenghong Zuo, Chengyong He
Format: Article
Language:English
Published: Wiley 2024-12-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202406343
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author Naying Zheng
Tingting Liao
Chuchu Zhang
Zheyang Zhang
Sen Yan
Xiaohan Xi
Fengkai Ruan
Chunyan Yang
Qingliang Zhao
Wenbo Deng
Jialiang Huang
Zi‐Tao Huang
Zhi‐Feng Chen
Xiang Wang
Qingming Qu
Zhenghong Zuo
Chengyong He
author_facet Naying Zheng
Tingting Liao
Chuchu Zhang
Zheyang Zhang
Sen Yan
Xiaohan Xi
Fengkai Ruan
Chunyan Yang
Qingliang Zhao
Wenbo Deng
Jialiang Huang
Zi‐Tao Huang
Zhi‐Feng Chen
Xiang Wang
Qingming Qu
Zhenghong Zuo
Chengyong He
author_sort Naying Zheng
collection DOAJ
description Abstract Quantum dots (QDs) are widely used, but their health impact on the visual system is little known. This study aims to elucidate the effects and mechanisms of typical metallic QDs on retinas using zebrafish. Comprehensive histology, imaging, and bulk RNA sequencing reveal that InP/ZnS QDs cause retinal degeneration. Furthermore, single‐cell RNA‐seq reveals a reduction in the number of retinal pigment epithelial cells (RPE) and short‐wave cone UV photoreceptor cells (PR(UV)), accompanied by an increase in middle‐ and long‐wave cone red, green, and blue photoreceptor cells [PR(RGB)]. Mechanistically, after endocytosis by RPE, InP/ZnS QDs inhibit the expression of splicing factor prpf8, resulting in gpx4b mRNA unsplicing, which finally decrease glutathione and induce ferroptosis and mitophagy. The decrease of RPE fails to engulf the damaged outer segments of PR, possibly promoting the differentiation of PR(UV) to PR(RGB). Knockout prpf8 or gpx4b with CRISPR/Cas9 system, the retinal damage is also observed. Whereas, overexpression of prpf8 or gpx4b, or supplement of glutathione can rescue the retinal degenerative damage caused by InP/ZnS QDs. In conclusion, this study illustrates the potential health risks of InP/ZnS QDs on eye development and provides valuable insights into the underlying mechanisms of InP/ZnS QDs‐caused retinal degeneration.
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spelling doaj-art-e0f9742b1f1d45bca589df1e1f1e5cdf2024-12-11T16:00:49ZengWileyAdvanced Science2198-38442024-12-011146n/an/a10.1002/advs.202406343Quantum Dots‐caused Retinal Degeneration in Zebrafish Regulated by Ferroptosis and Mitophagy in Retinal Pigment Epithelial Cells through Inhibiting SpliceosomeNaying Zheng0Tingting Liao1Chuchu Zhang2Zheyang Zhang3Sen Yan4Xiaohan Xi5Fengkai Ruan6Chunyan Yang7Qingliang Zhao8Wenbo Deng9Jialiang Huang10Zi‐Tao Huang11Zhi‐Feng Chen12Xiang Wang13Qingming Qu14Zhenghong Zuo15Chengyong He16Department of Ophthalmology in Xiang'an Hospital of Xiamen University State Key Laboratory of Cellular Stress Biology School of Life Sciences Faculty of Medicine and Life Sciences Xiamen University Xiamen Fujian 361102 ChinaDepartment of Ophthalmology in Xiang'an Hospital of Xiamen University State Key Laboratory of Cellular Stress Biology School of Life Sciences Faculty of Medicine and Life Sciences Xiamen University Xiamen Fujian 361102 ChinaDepartment of Ophthalmology in Xiang'an Hospital of Xiamen University State Key Laboratory of Cellular Stress Biology School of Life Sciences Faculty of Medicine and Life Sciences Xiamen University Xiamen Fujian 361102 ChinaDepartment of Ophthalmology in Xiang'an Hospital of Xiamen University State Key Laboratory of Cellular Stress Biology School of Life Sciences Faculty of Medicine and Life Sciences Xiamen University Xiamen Fujian 361102 ChinaDepartment of Chemistry State Key Laboratory of Physical Chemistry of Solid Surfaces Collaborative Innovation Center of Chemistry for Energy Materials (i‐ChEM) Innovation Laboratory for Sciences and Technologies of Energy Materials of Fujian Province (IKKEM) College of Chemistry and Chemical Engineering Xiamen University Xiamen 361005 ChinaDepartment of Chemistry State Key Laboratory of Physical Chemistry of Solid Surfaces Collaborative Innovation Center of Chemistry for Energy Materials (i‐ChEM) Innovation Laboratory for Sciences and Technologies of Energy Materials of Fujian Province (IKKEM) College of Chemistry and Chemical Engineering Xiamen University Xiamen 361005 ChinaDepartment of Ophthalmology in Xiang'an Hospital of Xiamen University State Key Laboratory of Cellular Stress Biology School of Life Sciences Faculty of Medicine and Life Sciences Xiamen University Xiamen Fujian 361102 ChinaDepartment of Ophthalmology in Xiang'an Hospital of Xiamen University State Key Laboratory of Cellular Stress Biology School of Life Sciences Faculty of Medicine and Life Sciences Xiamen University Xiamen Fujian 361102 ChinaState Key Laboratory of Vaccines for Infectious Diseases Center for Molecular Imaging and Translational Medicine Xiang An Biomedicine Laboratory School of Public Health Xiamen University Xiamen Fujian 361005 ChinaKey Laboratory of Reproductive Health Research Fujian Province University School of Medicine Xiamen University Xiamen Fujian 361005 ChinaDepartment of Ophthalmology in Xiang'an Hospital of Xiamen University State Key Laboratory of Cellular Stress Biology School of Life Sciences Faculty of Medicine and Life Sciences Xiamen University Xiamen Fujian 361102 ChinaGuangdong Key Laboratory of Environmental Catalysis and Health Risk Control Guangdong‐Hong Kong‐Macao Joint Laboratory for Contaminants Exposure and Health School of Environmental Science and Engineering Guangdong University of Technology Guangzhou 510006 ChinaGuangdong Key Laboratory of Environmental Catalysis and Health Risk Control Guangdong‐Hong Kong‐Macao Joint Laboratory for Contaminants Exposure and Health School of Environmental Science and Engineering Guangdong University of Technology Guangzhou 510006 ChinaDepartment of Chemistry State Key Laboratory of Physical Chemistry of Solid Surfaces Collaborative Innovation Center of Chemistry for Energy Materials (i‐ChEM) Innovation Laboratory for Sciences and Technologies of Energy Materials of Fujian Province (IKKEM) College of Chemistry and Chemical Engineering Xiamen University Xiamen 361005 ChinaDepartment of Ophthalmology in Xiang'an Hospital of Xiamen University State Key Laboratory of Cellular Stress Biology School of Life Sciences Faculty of Medicine and Life Sciences Xiamen University Xiamen Fujian 361102 ChinaDepartment of Ophthalmology in Xiang'an Hospital of Xiamen University State Key Laboratory of Cellular Stress Biology School of Life Sciences Faculty of Medicine and Life Sciences Xiamen University Xiamen Fujian 361102 ChinaDepartment of Ophthalmology in Xiang'an Hospital of Xiamen University State Key Laboratory of Cellular Stress Biology School of Life Sciences Faculty of Medicine and Life Sciences Xiamen University Xiamen Fujian 361102 ChinaAbstract Quantum dots (QDs) are widely used, but their health impact on the visual system is little known. This study aims to elucidate the effects and mechanisms of typical metallic QDs on retinas using zebrafish. Comprehensive histology, imaging, and bulk RNA sequencing reveal that InP/ZnS QDs cause retinal degeneration. Furthermore, single‐cell RNA‐seq reveals a reduction in the number of retinal pigment epithelial cells (RPE) and short‐wave cone UV photoreceptor cells (PR(UV)), accompanied by an increase in middle‐ and long‐wave cone red, green, and blue photoreceptor cells [PR(RGB)]. Mechanistically, after endocytosis by RPE, InP/ZnS QDs inhibit the expression of splicing factor prpf8, resulting in gpx4b mRNA unsplicing, which finally decrease glutathione and induce ferroptosis and mitophagy. The decrease of RPE fails to engulf the damaged outer segments of PR, possibly promoting the differentiation of PR(UV) to PR(RGB). Knockout prpf8 or gpx4b with CRISPR/Cas9 system, the retinal damage is also observed. Whereas, overexpression of prpf8 or gpx4b, or supplement of glutathione can rescue the retinal degenerative damage caused by InP/ZnS QDs. In conclusion, this study illustrates the potential health risks of InP/ZnS QDs on eye development and provides valuable insights into the underlying mechanisms of InP/ZnS QDs‐caused retinal degeneration.https://doi.org/10.1002/advs.202406343FerroptosisQuantum dotsRetinal degenerationSingle‐cell RNA sequencingSpliceosome
spellingShingle Naying Zheng
Tingting Liao
Chuchu Zhang
Zheyang Zhang
Sen Yan
Xiaohan Xi
Fengkai Ruan
Chunyan Yang
Qingliang Zhao
Wenbo Deng
Jialiang Huang
Zi‐Tao Huang
Zhi‐Feng Chen
Xiang Wang
Qingming Qu
Zhenghong Zuo
Chengyong He
Quantum Dots‐caused Retinal Degeneration in Zebrafish Regulated by Ferroptosis and Mitophagy in Retinal Pigment Epithelial Cells through Inhibiting Spliceosome
Advanced Science
Ferroptosis
Quantum dots
Retinal degeneration
Single‐cell RNA sequencing
Spliceosome
title Quantum Dots‐caused Retinal Degeneration in Zebrafish Regulated by Ferroptosis and Mitophagy in Retinal Pigment Epithelial Cells through Inhibiting Spliceosome
title_full Quantum Dots‐caused Retinal Degeneration in Zebrafish Regulated by Ferroptosis and Mitophagy in Retinal Pigment Epithelial Cells through Inhibiting Spliceosome
title_fullStr Quantum Dots‐caused Retinal Degeneration in Zebrafish Regulated by Ferroptosis and Mitophagy in Retinal Pigment Epithelial Cells through Inhibiting Spliceosome
title_full_unstemmed Quantum Dots‐caused Retinal Degeneration in Zebrafish Regulated by Ferroptosis and Mitophagy in Retinal Pigment Epithelial Cells through Inhibiting Spliceosome
title_short Quantum Dots‐caused Retinal Degeneration in Zebrafish Regulated by Ferroptosis and Mitophagy in Retinal Pigment Epithelial Cells through Inhibiting Spliceosome
title_sort quantum dots caused retinal degeneration in zebrafish regulated by ferroptosis and mitophagy in retinal pigment epithelial cells through inhibiting spliceosome
topic Ferroptosis
Quantum dots
Retinal degeneration
Single‐cell RNA sequencing
Spliceosome
url https://doi.org/10.1002/advs.202406343
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