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The insecticide permethrin induces transgenerational behavioral changes linked to transcriptomic and epigenetic alterations in zebrafish (Danio rerio)

Authors :
Xavier Cousin
Christoph Grunau
Steffen Keiter
Joëlle Rüegg
Nikolai Scherbak
Philipp Antczak
Mélanie Blanc
Man-Technology-Environment Research Centre, School of Science and Technology
Örebro University
MARine Biodiversity Exploitation and Conservation (UMR MARBEC)
Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)
Génétique Animale et Biologie Intégrative (GABI)
Université Paris-Saclay-AgroParisTech-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Centre for Molecular Medicine Cologne [Cologne] (CMMC)
University Hospital of Cologne [Cologne]
Interactions Hôtes-Pathogènes-Environnements (IHPE)
Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Perpignan Via Domitia (UPVD)
Department of Organismal Biology
Uppsala University
This study was supported by the Enforce laboratory, funded by the Knowledge Foundation (KK Stiftelsen 20160019, Sweden), and by the Helge Ax:Son Foundation (F19-0339, Sweden). RRBS experiments were performed at the Environmental Epigenetics facility of IHPE with the support of LabEx CeMEB, an Agence Nationale de la Recherche (ANR) 'Investissements d'avenir' program (ANR-10-LABX-04-01, France).
ANR-10-LABX-0004,CeMEB,Mediterranean Center for Environment and Biodiversity(2010)
AgroParisTech-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Université de Perpignan Via Domitia (UPVD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)
Source :
Science of the Total Environment, Science of the Total Environment, Elsevier, 2021, 779, pp.146404. ⟨10.1016/j.scitotenv.2021.146404⟩, Science of the Total Environment, 2021, 779, pp.146404. ⟨10.1016/j.scitotenv.2021.146404⟩, Science Of The Total Environment (0048-9697) (Elsevier BV), 2021-07, Vol. 779, P. 146404 (11p.)
Publication Year :
2021
Publisher :
HAL CCSD, 2021.

Abstract

International audience; The pyrethroid insecticide permethrin is widely used for agricultural and domestic purposes. Previous data indicated that it acts as a developmental neurotoxicant and can induce transgenerational effects in non-target organisms. However, associated underlying mechanisms remain unclear. The aim of this study was to investigate permethrin-related transgenerational effects in the zebrafish model, and to identify possible molecular mechanisms underlying inheritance. Zebrafish (F0) were exposed to permethrin during early-life (2 hours postfertilization up to 28 days). The F1 and F2 offspring generations were obtained by pairing exposed F0 males and females, and were bred unexposed. Locomotor and anxiety behavior were investigated, together with transcriptomic and epigenomic (DNA methylation) changes in brains. Permethrin exposed F0 fish were hypoactive at adulthood, while males from the F1 and F2 generations showed a specific decrease in anxiety-like behavior. In F0, transcriptomic data showed enrichment in pathways related to glutamatergic synapse activity, which may partly underlie the behavioral effects. In F1 and F2 males, dysregulation of similar pathways was observed, including a subset of differentially methylated regions that were inherited from the F0 to the F2 generation and indicated stable dysregulation of glutamatergic signaling. Altogether, the present results provide novel evidence on the transgenerational neurotoxic effects of permethrin, as well as mechanistic insight: a transient exposure induces persistent transcriptional and DNA methylation changes that may translate into transgenerational alteration of glutamatergic signaling and, thus, into behavioral alterations.

Details

Language :
English
ISSN :
00489697 and 18791026
Database :
OpenAIRE
Journal :
Science of the Total Environment, Science of the Total Environment, Elsevier, 2021, 779, pp.146404. ⟨10.1016/j.scitotenv.2021.146404⟩, Science of the Total Environment, 2021, 779, pp.146404. ⟨10.1016/j.scitotenv.2021.146404⟩, Science Of The Total Environment (0048-9697) (Elsevier BV), 2021-07, Vol. 779, P. 146404 (11p.)
Accession number :
edsair.doi.dedup.....72a48ca2fcbcc8f32fc862c1c2fcc6d3
Full Text :
https://doi.org/10.1016/j.scitotenv.2021.146404⟩