Development of a transcription-based bioanalytical tool to quantify the toxic potencies of hydrophilic compounds in water using the nematode Caenorhabditis elegans

Low concentrations of environmental contaminants can be difficult to detect with current analytical tools, yet they may pose a risk to human and environmental health. The development of bioanalytical tools can help to quantify toxic potencies of biologically active compounds even of hydrophilic cont...

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Autores principales: Antoine Karengera, Cong Bao, Joost A.G. Riksen, H. Pieter J. van Veelen, Mark G. Sterken, Jan E. Kammenga, Albertinka J. Murk, Inez J.T. Dinkla
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Publicado: Elsevier 2021
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spelling oai:doaj.org-article:ce274979273c4dc7a6cb7fdc458be96a2021-11-06T04:17:34ZDevelopment of a transcription-based bioanalytical tool to quantify the toxic potencies of hydrophilic compounds in water using the nematode Caenorhabditis elegans0147-651310.1016/j.ecoenv.2021.112923https://doaj.org/article/ce274979273c4dc7a6cb7fdc458be96a2021-12-01T00:00:00Zhttp://www.sciencedirect.com/science/article/pii/S0147651321010356https://doaj.org/toc/0147-6513Low concentrations of environmental contaminants can be difficult to detect with current analytical tools, yet they may pose a risk to human and environmental health. The development of bioanalytical tools can help to quantify toxic potencies of biologically active compounds even of hydrophilic contaminants that are hard to extract from water samples. In this study, we exposed the model organism Caenorhabditis elegans synchronized in larval stage L4 to hydrophilic compounds via the water phase and analyzed the effect on gene transcription abundance. The nematodes were exposed to three direct-acting genotoxicants (1 mM and 5 mM): N-ethyl-N-nitrosourea (ENU), formaldehyde (HCHO), and methyl methanesulfonate (MMS). Genome-wide gene expression analysis using microarrays revealed significantly altered transcription levels of 495 genes for HCHO, 285 genes for ENU, and 569 genes for MMS in a concentration-dependent manner. A relatively high number of differentially expressed genes was downregulated, suggesting a general stress in nematodes treated with toxicants. Gene ontology and Kyoto encyclopedia of genes and genomes analysis demonstrated that the upregulated genes were primarily associated with metabolism, xenobiotic detoxification, proteotoxic stress, and innate immune response. Interestingly, genes downregulated by MMS were linked to the inhibition of neurotransmission, and this is in accordance with the observed decreased locomotion in MMS-exposed nematodes. Unexpectedly, the expression level of DNA damage response genes such as cell-cycle checkpoints or DNA-repair proteins were not altered. Overall, the current study shows that gene expression profiling of nematodes can be used to identify the potential mechanisms underlying the toxicity of chemical compounds. C. elegans is a promising test organism to further develop into a bioanalytical tool for quantification of the toxic potency of a wide array of hydrophilic contaminants.Antoine KarengeraCong BaoJoost A.G. RiksenH. Pieter J. van VeelenMark G. SterkenJan E. KammengaAlbertinka J. MurkInez J.T. DinklaElsevierarticleCaenorhabditis elegansGenotoxicantsBioanalytical toolGene expressionHydrophilicNematodeEnvironmental pollutionTD172-193.5Environmental sciencesGE1-350ENEcotoxicology and Environmental Safety, Vol 227, Iss , Pp 112923- (2021)
institution DOAJ
collection DOAJ
language EN
topic Caenorhabditis elegans
Genotoxicants
Bioanalytical tool
Gene expression
Hydrophilic
Nematode
Environmental pollution
TD172-193.5
Environmental sciences
GE1-350
spellingShingle Caenorhabditis elegans
Genotoxicants
Bioanalytical tool
Gene expression
Hydrophilic
Nematode
Environmental pollution
TD172-193.5
Environmental sciences
GE1-350
Antoine Karengera
Cong Bao
Joost A.G. Riksen
H. Pieter J. van Veelen
Mark G. Sterken
Jan E. Kammenga
Albertinka J. Murk
Inez J.T. Dinkla
Development of a transcription-based bioanalytical tool to quantify the toxic potencies of hydrophilic compounds in water using the nematode Caenorhabditis elegans
description Low concentrations of environmental contaminants can be difficult to detect with current analytical tools, yet they may pose a risk to human and environmental health. The development of bioanalytical tools can help to quantify toxic potencies of biologically active compounds even of hydrophilic contaminants that are hard to extract from water samples. In this study, we exposed the model organism Caenorhabditis elegans synchronized in larval stage L4 to hydrophilic compounds via the water phase and analyzed the effect on gene transcription abundance. The nematodes were exposed to three direct-acting genotoxicants (1 mM and 5 mM): N-ethyl-N-nitrosourea (ENU), formaldehyde (HCHO), and methyl methanesulfonate (MMS). Genome-wide gene expression analysis using microarrays revealed significantly altered transcription levels of 495 genes for HCHO, 285 genes for ENU, and 569 genes for MMS in a concentration-dependent manner. A relatively high number of differentially expressed genes was downregulated, suggesting a general stress in nematodes treated with toxicants. Gene ontology and Kyoto encyclopedia of genes and genomes analysis demonstrated that the upregulated genes were primarily associated with metabolism, xenobiotic detoxification, proteotoxic stress, and innate immune response. Interestingly, genes downregulated by MMS were linked to the inhibition of neurotransmission, and this is in accordance with the observed decreased locomotion in MMS-exposed nematodes. Unexpectedly, the expression level of DNA damage response genes such as cell-cycle checkpoints or DNA-repair proteins were not altered. Overall, the current study shows that gene expression profiling of nematodes can be used to identify the potential mechanisms underlying the toxicity of chemical compounds. C. elegans is a promising test organism to further develop into a bioanalytical tool for quantification of the toxic potency of a wide array of hydrophilic contaminants.
format article
author Antoine Karengera
Cong Bao
Joost A.G. Riksen
H. Pieter J. van Veelen
Mark G. Sterken
Jan E. Kammenga
Albertinka J. Murk
Inez J.T. Dinkla
author_facet Antoine Karengera
Cong Bao
Joost A.G. Riksen
H. Pieter J. van Veelen
Mark G. Sterken
Jan E. Kammenga
Albertinka J. Murk
Inez J.T. Dinkla
author_sort Antoine Karengera
title Development of a transcription-based bioanalytical tool to quantify the toxic potencies of hydrophilic compounds in water using the nematode Caenorhabditis elegans
title_short Development of a transcription-based bioanalytical tool to quantify the toxic potencies of hydrophilic compounds in water using the nematode Caenorhabditis elegans
title_full Development of a transcription-based bioanalytical tool to quantify the toxic potencies of hydrophilic compounds in water using the nematode Caenorhabditis elegans
title_fullStr Development of a transcription-based bioanalytical tool to quantify the toxic potencies of hydrophilic compounds in water using the nematode Caenorhabditis elegans
title_full_unstemmed Development of a transcription-based bioanalytical tool to quantify the toxic potencies of hydrophilic compounds in water using the nematode Caenorhabditis elegans
title_sort development of a transcription-based bioanalytical tool to quantify the toxic potencies of hydrophilic compounds in water using the nematode caenorhabditis elegans
publisher Elsevier
publishDate 2021
url https://doaj.org/article/ce274979273c4dc7a6cb7fdc458be96a
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