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

Type Article
Date 2021-07
Language English
Author(s) Blanc Mélanie1, 2, 3, Antczak Philipp4, Cousin XavierORCID2, 3, Grunau Christoph5, Scherbak Nikolai1, 6, Rüegg Joëlle7, Keiter Steffen H.1
Affiliation(s) 1 : Man-Technology-Environment Research Centre (MTM), School of Science and Technology, Örebro University, Fakultetsgatan 1, S-701 82 Örebro, Sweden
2 : MARBEC, University of Montpellier, CNRS, Ifremer, IRD, Palavas, France
3 : Université Paris-Saclay, AgroParisTech, INRAE, GABI, Domaine de Vilvert, F-78350 Jouy-en-Josas, France
4 : Centre for Molecular Medicine Cologne, University of Cologne, 50931 Cologne, German
5 : IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Perpignan, France
6 : Örebro Life Science Centre, School of Science and Technology, Örebro University, Fakultetsgatan 1, S-701 82 Örebro, Sweden
7 : Department of Organismal Biology, Uppsala University, Norbyv. 18A, 75236 Uppsala, Sweden
Source Science of The Total Environment (00489697) (Elsevier BV), 2021-07 , Vol. 77+ , P. 146404 (11p.)
DOI 10.1016/j.scitotenv.2021.146404
Keyword(s) Transgenerational epigenetic inheritance, developmental neurotoxicity, glutamatergic signaling, DNA methylation, pesticide
Abstract

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 h post-fertilization 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.

Full Text
File Pages Size Access
Publisher's official version 37 1 MB Open access
Supplementary material 1 1 MB Open access
Supplementary material 2 411 KB Open access
Top of the page

How to cite 

Blanc Mélanie, Antczak Philipp, Cousin Xavier, Grunau Christoph, Scherbak Nikolai, Rüegg Joëlle, Keiter Steffen H. (2021). The insecticide permethrin induces transgenerational behavioral changes linked to transcriptomic and epigenetic alterations in zebrafish (Danio rerio). Science of The Total Environment, 77+, 146404 (11p.). Publisher's official version : https://doi.org/10.1016/j.scitotenv.2021.146404 , Open Access version : https://archimer.ifremer.fr/doc/00685/79661/