Dataset Information

Paternal exposure to a common herbicide alters the behavior and serotonergic system of zebrafish offspring.

ABSTRACT: Increasingly, studies are revealing that endocrine disrupting chemicals (EDCs) can alter animal behavior. Early life exposure to EDCs may permanently alter phenotypes through to adulthood. In addition, the effects of EDCs may not be isolated to a single generation - offspring may indirectly be impacted, via non-genetic processes. Here, we analyzed the effects of paternal atrazine exposure on behavioral traits (distance moved, exploration, bottom-dwelling time, latency to enter the top zone, and interaction with a mirror) and whole-brain mRNA of genes involved in the serotonergic system regulation (slc6a4a, slc6a4b, htr1Aa, htr1B, htr2B) of zebrafish (Danio rerio). F0 male zebraFIsh were exposed to atrazine at 0.3, 3 or 30 part per billion (ppb) during early juvenile development, the behavior of F1 progeny was tested at adulthood, and the effect of 0.3 ppb atrazine treatment on mRNA transcription was quantified. Paternal exposure to atrazine significantly reduced interactions with a mirror (a proxy for aggression) and altered the latency to enter the top zone of a tank in unexposed F1 offspring. Bottom-dwelling time (a proxy for anxiety) also appeared to be somewhat affected, and activity (distance moved) was reduced in the context of aggression. slc6a4a and htr1Aa mRNA transcript levels were found to correlate positively with anxiety levels in controls, but we found that this relationship was disrupted in the 0.3 ppb atrazine treatment group. Overall, paternal atrazine exposure resulted in alterations across a variety of behavioral traits and showed signs of serotonergic system dysregulation, demonstrating intergenerational effects. Further research is needed to explore transgenerational effects on behavior and possible mechanisms underpinning behavioral effects.

SUBMITTER: Lamb SD

PROVIDER: S-EPMC7147785 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Paternal exposure to a common herbicide alters the behavior and serotonergic system of zebrafish offspring.

Lamb Simon D SD Chia Jolyn H Z JHZ Johnson Sheri L SL

PloS one 20200410 4

Increasingly, studies are revealing that endocrine disrupting chemicals (EDCs) can alter animal behavior. Early life exposure to EDCs may permanently alter phenotypes through to adulthood. In addition, the effects of EDCs may not be isolated to a single generation - offspring may indirectly be impacted, via non-genetic processes. Here, we analyzed the effects of paternal atrazine exposure on behavioral traits (distance moved, exploration, bottom-dwelling time, latency to enter the top zone, and ...[more]

PMID: 32275662

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Project description:Recent studies have suggested that physiological and behavioral traits may be transgenerationally inherited through the paternal lineage, possibly via non-genomic signals derived from the sperm. To investigate how paternal stress might influence offspring behavioral phenotypes, a model of hypothalamic-pituitary-adrenal (HPA) axis dysregulation was used. Male breeders were administered water supplemented with corticosterone (CORT) for 4 weeks before mating with untreated female mice. Female, but not male, F1 offspring of CORT-treated fathers displayed altered fear extinction at 2 weeks of age. Only male F1 offspring exhibited altered patterns of ultrasonic vocalization at postnatal day 3 and, as adults, showed decreased time in open on the elevated-plus maze and time in light on the light-dark apparatus, suggesting a hyperanxiety-like behavioral phenotype due to paternal CORT treatment. Interestingly, expression of the paternally imprinted gene Igf2 was increased in the hippocampus of F1 male offspring but downregulated in female offspring. Male and female F2 offspring displayed increased time spent in the open arm of the elevated-plus maze, suggesting lower levels of anxiety compared with control animals. Only male F2 offspring showed increased immobility time on the forced-swim test and increased latency to feed on the novelty-supressed feeding test, suggesting a depression-like phenotype in these animals. Collectively, these data provide evidence that paternal CORT treatment alters anxiety and depression-related behaviors across multiple generations. Analysis of the small RNA profile in sperm from CORT-treated males revealed marked effects on the expression of small noncoding RNAs. Sperm from CORT-treated males contained elevated levels of three microRNAs, miR-98, miR-144 and miR-190b, which are predicted to interact with multiple growth factors, including Igf2 and Bdnf. Sustained elevation of glucocorticoids is therefore involved in the transmission of paternal stress-induced traits across generations in a process involving small noncoding RNA signals transmitted by the male germline.

Dataset Information

Paternal exposure to a common herbicide alters the behavior and serotonergic system of zebrafish offspring.

Publications

Paternal exposure to a common herbicide alters the behavior and serotonergic system of zebrafish offspring.

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