Zebrafish exposure to environmentally relevant concentration of depleted uranium impairs progeny development at the molecular and histological levels

Abstract

Uranium is an actinide naturally found in the environment. Anthropogenic activities lead to the release of increasing amounts of uranium and depleted uranium (DU) in the environment, posing potential risks to aquatic organisms due to radiological and chemical toxicity of this radionucleide. Although environmental contaminations with high levels of uranium have already been observed, chronic exposures of non-human species to levels close to the environmental quality standards remain scarcely characterized. The present study focused on the identification of the molecular pathways impacted by a chronic exposure of zebrafish to 20 μg/L of DU during 10 days. The transcriptomic effects were evaluated by the use of the mRNAseq analysis in three organs of adult zebrafish, the brain the testis and the ovaries, and two developmental stages of the adult fish progeny, two-cells embryo and four-days larvae. The results highlight generic effects on the cell adhesion process, but also specific transcriptomic responses depending on the organ or the developmental stage investigated. The analysis of the transgenerational effects of DU-exposure on the four-day zebrafish larvae demonstrate an induction of genes involved in oxidative response (cat, mpx, sod1 and sod2), a decrease of expression of the two hatching enzymes (he1a and he1b), the deregulation of the expression of gene coding for the ATPase complex and the induction of cellular stress. Electron microscopy analysis of skeletal muscles on the four-days larvae highlights significant histological impacts on the ultrastructure of both the mitochondria and the myofibres. In addition, the comparison with the transcriptomic data obtained for the acetylcholine esterase mutant reveals the induction of protein-chaperons in the skeletal muscles of the progeny of fish chronically exposed to DU, pointing towards long lasting effects of this chemical in the muscles. The results presented in this study support the hypothesis that a chronic parental exposure to an environmentally relevant concentration of DU could impair the progeny development with significant effects observed both at the molecular level and on the histological ultrastructure of organs. This study provides a comprehensive transcriptomic dataset useful for ecotoxicological studies on other fish species at the molecular level. It also provides a key DU responsive gene, egr1, which may be a candidate biomarker for monitoring aquatic pollution by heavy metals.

Whole transcriptome data of zebrafish exposed to chronic dose of depleted uranium

“…We describe in this article the summary statistics of the differential gene expression analysis and focus on key molecular pathways affected by an exposure to a low concentration of DU. The data presented in this study supports the observation made in Armant et al (2017) [1] ( https://doi.org/10.1016/j.dib.2016.05.007 ) that DU can induce a molecular stress in both adult zebrafish and their progeny. The raw dataset has been deposited at the Gene Expression Omnibus (GEO) repository under the accession number GEO: GSE96603 .…”

“…This data consists of 35 high-throughput sequencing samples of adult brain, testis and ovaries obtained from adult zebrafish exposed to 20 µg/L of depleted uranium (DU) for 10 days, as well as their progeny both at the two-cells stage and four-days larvae (96 h post-fertilization, hpf) [1] , [2] . The data are deposited under the Gene Expression Omnibus (GEO) number GEO: GSE96603 at http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE96603 .…”

Uranium transfer and accumulation in organs of Danio rerio after waterborne exposure alone or combined with diet‐borne exposure

“…More than 50% of the total U burden in the internal organs (i.e., excluding the intestine and gill burdens) was measured in the testes after 20 d of both exposure pathways (Figure ). Uranium accumulation in the testes may confirm the epigenetic effects, transcriptomic changes, and histological damage (at higher levels of U exposure) in this organ detected by Bourrachot et al (), Gombeau et al (), and Armant et al ().…”

The toxicological mechanisms and detoxification of depleted uranium exposure

“…Uranium may cause behavioral changes and affect the circadian rhythm, locomotion, and cognitive functions in [ 11 ]. Chronic DU exposure has been shown to affect the genetic pathway involved in visual perception in zebrafish and to modify the transcriptomic pattern in this brain area [ 15 ]. In humans, however, a relationship between DU exposure and behavior changes has not been established.…”

“…Rodents exhibited testicular histopathological abnormalities and decreases in pregnancy rates and spermatid numbers after a chronic dose of 10–80 mg/kg/day uranium [ 13 , 14 ]. Armant et al [ 15 ] demonstrated that chronic parental exposure to 20 μg/L DU could impair the histological ultrastructure of organs and molecular development in zebrafish progeny.…”