Zinc oxide nanoparticles disrupt development and function of the olfactory sensory system impairing olfaction-mediated behaviour in zebrafish
Zinc (Zn) is an essential metal present in numerous enzymes throughout the body, playing a vital role in animal and human health. However, the increasing use of zinc oxide nanomaterials (ZnONPs) in a diverse range of products has raised concerns regarding their potential impacts on health and the en...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2023-10-01
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| Series: | Environment International |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S0160412023005007 |
| _version_ | 1797659948972244992 |
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| author | Aya Takesono Sylvia Dimitriadou Nathaniel J. Clark Richard D. Handy Sulayman Mourabit Matthew J. Winter Tetsuhiro Kudoh Charles R. Tyler |
| author_facet | Aya Takesono Sylvia Dimitriadou Nathaniel J. Clark Richard D. Handy Sulayman Mourabit Matthew J. Winter Tetsuhiro Kudoh Charles R. Tyler |
| author_sort | Aya Takesono |
| collection | DOAJ |
| description | Zinc (Zn) is an essential metal present in numerous enzymes throughout the body, playing a vital role in animal and human health. However, the increasing use of zinc oxide nanomaterials (ZnONPs) in a diverse range of products has raised concerns regarding their potential impacts on health and the environment. Despite these concerns, the toxicity of ZnONP exposure on animal health remain poorly understood. To help address this knowledge gap, we have developed a highly sensitive oxidative stress (OS) biosensor zebrafish capable of detecting cell/tissue-specific OS responses to low doses of various oxidative stressors, including Zn, in a live fish embryo.Using live-imaging analysis with this biosensor zebrafish embryo, we discovered that the olfactory sensory neurons in the brain are especially sensitive to ZnOP exposure. Furthermore, through studies monitoring neutrophil migration and neuronal activation in the embryonic brain and via behaviour analysis, we have found that sub-lethal doses of ZnONPs (ranging from 0.033 to 1 mg/L nominal concentrations), which had no visible effect on embryo growth or morphology, cause significant localised inflammation, disrupting the neurophysiology of olfactory brain tissues and ultimately impaired olfaction-mediated behaviour. Collectively, these findings establish a potent and important effect mechanism for ZnONP toxicity, indicating the olfactory sensory system as the primary target for ZnONPs as an environmental toxicant in aquatic environments. Our result also highlights that even low doses of ZnONPs can have detrimental effects on the olfactory sensory system, surpassing previous expectations. The importance of olfaction in environment sensing, sex behaviours and overall fitness across species raises concerns about the potential impact of ZnONPs on olfaction-mediated brain function and behaviour in animals and humans. Our study emphasises the need for greater consideration of the potential risks associated with these nanomaterials. |
| first_indexed | 2024-03-11T18:23:34Z |
| format | Article |
| id | doaj.art-f22f5e6b85b140d8ab1048f91c0a3700 |
| institution | Directory Open Access Journal |
| issn | 0160-4120 |
| language | English |
| last_indexed | 2024-03-11T18:23:34Z |
| publishDate | 2023-10-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Environment International |
| spelling | doaj.art-f22f5e6b85b140d8ab1048f91c0a37002023-10-15T04:36:32ZengElsevierEnvironment International0160-41202023-10-01180108227Zinc oxide nanoparticles disrupt development and function of the olfactory sensory system impairing olfaction-mediated behaviour in zebrafishAya Takesono0Sylvia Dimitriadou1Nathaniel J. Clark2Richard D. Handy3Sulayman Mourabit4Matthew J. Winter5Tetsuhiro Kudoh6Charles R. Tyler7Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, Devon EX4 4QD, United Kingdom; Corresponding authors.Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, Devon EX4 4QD, United KingdomFaculty of Science and Engineering, School of Biological and Marine Sciences, University of Plymouth, Drake Circus, Plymouth PL4 8AA, United KingdomFaculty of Science and Engineering, School of Biological and Marine Sciences, University of Plymouth, Drake Circus, Plymouth PL4 8AA, United KingdomBiosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, Devon EX4 4QD, United KingdomBiosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, Devon EX4 4QD, United KingdomBiosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, Devon EX4 4QD, United KingdomBiosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, Devon EX4 4QD, United Kingdom; Corresponding authors.Zinc (Zn) is an essential metal present in numerous enzymes throughout the body, playing a vital role in animal and human health. However, the increasing use of zinc oxide nanomaterials (ZnONPs) in a diverse range of products has raised concerns regarding their potential impacts on health and the environment. Despite these concerns, the toxicity of ZnONP exposure on animal health remain poorly understood. To help address this knowledge gap, we have developed a highly sensitive oxidative stress (OS) biosensor zebrafish capable of detecting cell/tissue-specific OS responses to low doses of various oxidative stressors, including Zn, in a live fish embryo.Using live-imaging analysis with this biosensor zebrafish embryo, we discovered that the olfactory sensory neurons in the brain are especially sensitive to ZnOP exposure. Furthermore, through studies monitoring neutrophil migration and neuronal activation in the embryonic brain and via behaviour analysis, we have found that sub-lethal doses of ZnONPs (ranging from 0.033 to 1 mg/L nominal concentrations), which had no visible effect on embryo growth or morphology, cause significant localised inflammation, disrupting the neurophysiology of olfactory brain tissues and ultimately impaired olfaction-mediated behaviour. Collectively, these findings establish a potent and important effect mechanism for ZnONP toxicity, indicating the olfactory sensory system as the primary target for ZnONPs as an environmental toxicant in aquatic environments. Our result also highlights that even low doses of ZnONPs can have detrimental effects on the olfactory sensory system, surpassing previous expectations. The importance of olfaction in environment sensing, sex behaviours and overall fitness across species raises concerns about the potential impact of ZnONPs on olfaction-mediated brain function and behaviour in animals and humans. Our study emphasises the need for greater consideration of the potential risks associated with these nanomaterials.http://www.sciencedirect.com/science/article/pii/S0160412023005007Nano-metal pollutionOxidative stressBiosensor transgenic zebrafishDevelopmental neurotoxicityAdverse Outcome Pathway (AOP) |
| spellingShingle | Aya Takesono Sylvia Dimitriadou Nathaniel J. Clark Richard D. Handy Sulayman Mourabit Matthew J. Winter Tetsuhiro Kudoh Charles R. Tyler Zinc oxide nanoparticles disrupt development and function of the olfactory sensory system impairing olfaction-mediated behaviour in zebrafish Environment International Nano-metal pollution Oxidative stress Biosensor transgenic zebrafish Developmental neurotoxicity Adverse Outcome Pathway (AOP) |
| title | Zinc oxide nanoparticles disrupt development and function of the olfactory sensory system impairing olfaction-mediated behaviour in zebrafish |
| title_full | Zinc oxide nanoparticles disrupt development and function of the olfactory sensory system impairing olfaction-mediated behaviour in zebrafish |
| title_fullStr | Zinc oxide nanoparticles disrupt development and function of the olfactory sensory system impairing olfaction-mediated behaviour in zebrafish |
| title_full_unstemmed | Zinc oxide nanoparticles disrupt development and function of the olfactory sensory system impairing olfaction-mediated behaviour in zebrafish |
| title_short | Zinc oxide nanoparticles disrupt development and function of the olfactory sensory system impairing olfaction-mediated behaviour in zebrafish |
| title_sort | zinc oxide nanoparticles disrupt development and function of the olfactory sensory system impairing olfaction mediated behaviour in zebrafish |
| topic | Nano-metal pollution Oxidative stress Biosensor transgenic zebrafish Developmental neurotoxicity Adverse Outcome Pathway (AOP) |
| url | http://www.sciencedirect.com/science/article/pii/S0160412023005007 |
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