Transcriptomic changes underlie altered egg protein production and reduced fecundity in an estuarine model fish exposed to bifenthrin

Brander, Susanne M.; Jeffries, Ken M.; Cole, Bryan J.; DeCourten, Bethany M.; White, J. Wilson; Hasenbein, Simone; Fangue, Nann A.; Connon, Richard E.

doi:10.1016/j.aquatox.2016.02.014

Cited by 77 publications

(87 citation statements)

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“…This range of concentrations was chosen to reflect bifenthrin concentrations measured in Californian surface waters (Weston and Lydy, 2012), and earlier assessments of bifenthrin exposure with inland silversides (Brander et al, 2012b; DeGroot and Brander, 2014; Brander et al, 2016). Methanol was used as a solvent carrier for the bifenthrin treatments.…”

Section: Methodsmentioning

confidence: 99%

“…Bioaccumulation of bifenthrin in tissues has also been demonstrated (Munaretto et al, 2013) potentially leading to long-term, or delayed effects resulting from developmental exposure. Endocrine disruption in response to bifenthrin (ng/L) has been repeatedly determined in inland silversides ( Menidia beryllina ), with significant impacts at concentrations ranging from 0.5 to 50 ng/L (Brander et al, 2012b; DeGroot and Brander, 2014; Brander et al, 2016; DeCourten and Brander, 2017). Interestingly, bifenthrin metabolites appear to contribute most to the estrogenic effects (DeGroot and Brander, 2014), and responses can be greater at lower concentrations.…”

Section: Introductionmentioning

confidence: 99%

“…Interestingly, bifenthrin metabolites appear to contribute most to the estrogenic effects (DeGroot and Brander, 2014), and responses can be greater at lower concentrations. Studies investigating reproductive output with adult inland silversides determined a significant reduction when they were exposed to 0.5 ng/L for 21 days (Brander et al, 2016). The influences of 1 ng/L bifenthrin were further evaluated in a generation overlapping assay at both ambient and warmer temperatures, showing influences on sex ratios in the F1 generation and decreased viable offspring and deformities in F1 and F2 generation (DeCourten and Brander, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…While it has been repeatedly demonstrated that environmentally relevant concentrations of bifenthrin act as endocrine disruptors (Brander et al, 2016), little is known about how these concentrations can impact neurological and behavior endpoints in fishes; a knowledge gap that needs to be addressed, since endocrine disruption has been linked to adverse neurodevelopmental outcomes in other vertebrates (Segner, 2009; Masuo and Ishido, 2011; Frye et al, 2012). It has been suggested that behavioral endpoints, including performance associated with predator avoidance, are more informative in the evaluation of ecological effects of toxicants than long-established endpoints used in pesticide regulation, such as growth and mortality.…”

Section: Introductionmentioning

confidence: 99%

“…It is a well-suited species for ecotoxicological assessments representative of both freshwater and estuarine environments, for which it was developed as a model organism (Brander et al, 2012b). Several transcriptomic assessments have recently been conducted for this species (Jeffries et al, 2015a; Brander et al, 2016; DeCourten et al, 2018), providing a fundamental collection of RNA sequences towards the development of targeted molecular pathway assessments, such as the one presented herein.…”

Section: Introductionmentioning

confidence: 99%

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Developmental exposure to environmentally relevant concentrations of bifenthrin alters transcription of mTOR and ryanodine receptor-dependent signaling molecules and impairs predator avoidance behavior across early life stages in inland silversides (Menidia beryllina)

et al. 2019

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Altered transcription of calcium-dependent signaling cascades involving the ryanodine receptor (RyR) and mechanistic target of rapamycin (mTOR) in response to environmental exposures have been described in model vertebrates, including zebrafish, while the relevance for wild fishes remains unknown. To address this knowledge gap, we exposed the euryhaline model species Menidia beryllina (inland silversides) to the insecticide bifenthrin, a known modulator of calcium signaling. The main objectives of this study were to determine: (1) whether exposure of developing silversides to environmentally relevant concentrations of bifenthrin alters their behavior; and (2) whether behavioral changes correlate with altered expression of genes involved in RyR and mTOR-dependent signaling pathways. At six hours post fertilization (hpf), inland silversides were exposed to bifenthrin at 3, 27 and 122 ng/L until 7 days post fertilization (dpf, larvae hatched at 6dpf), followed by a 14-day recovery period in uncontaminated water. Transcriptional responses were measured at 5, 7 and 21 dpf; locomotor behavior following external stimuli and response to an olfactory predator cue were assessed at 7 and 21 dpf. Bifenthrin elicited significant non-monotonic transcriptional responses in the majority of genes examined at 5 dpf and at 21 dpf. Bifenthrin also significantly altered predator avoidance behavior via olfactory mechanisms with main effects identified for animals exposed to 3 and 27 ng/L. Behavioral effects were not detected in response to visual stimuli during acute exposure, but were significant in the predator-cue assessment following the recovery period, suggesting delayed and long-term effects of early developmental exposures to bifenthrin. Our findings demonstrate that at picomolar (pM) concentrations, which are often not represented in ecotoxicological studies, bifenthrin perturbs early development of inland silversides. These developmental impacts are manifested behaviorally at later life stages, specifically as altered patterns of predator avoidance behavior, which have been correlated with population decline. Collectively, these data suggest that bifenthrin may be negatively impacting wild fish populations.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Developmental exposure to environmentally relevant concentrations of bifenthrin alters transcription of mTOR and ryanodine receptor-dependent signaling molecules and impairs predator avoidance behavior across early life stages in inland silversides (Menidia beryllina)

et al. 2019

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Effects of bifenthrin exposure on the estrogenic and dopaminergic pathways in zebrafish embryos and juveniles

Bertotto

Richards

Gan

et al. 2017

Enviro Toxic and Chemistry

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Bifenthrin is a pyrethroid insecticide used in urban and agricultural applications. Previous studies have shown that environmentally relevant (ng/L) concentrations of bifenthrin increased plasma concentrations of 17b-estradiol (E2) and altered the expression of dopaminergic pathway components. The dopaminergic neurons can indirectly regulate E2 biosynthesis, suggesting that bifenthrin may disrupt the hypothalamic-pituitary-gonadal (HPG) axis. Because embryos do not have a complete HPG axis, the hypothesis that bifenthrin impairs dopamine regulation was tested in embryonic and 1-mo-old juvenile zebrafish (Danio rerio) with exposure to measured concentrations of 0.34 and 3.1 mg/L bifenthrin for 96 h. Quantitative reverse transcriptase polymerase chain reaction was used to investigate transcripts of tyrosine hydroxylase (TH), dopamine receptor 1 (DR1) and 2A (DR2A), dopamine active transporter (DAT), estrogen receptor a (ERa), ERb1, ERb2, luteinizing hormone b (LHb), follicle-stimulating hormone b (FSHb), vitellogenin (VTG), cytochrome P450 cyp19a1a, and cyp19a1b. Levels of E2 were measured by enzyme-linked immunosorbent assay (ELISA). Dopamine and its metabolites 3,4-dihydroxyphenylacetic acid (DOPAC) and homovanillic acid (HVA) concentrations were measured by liquid chromatrography-tandem mass spectrometry (LC-MS/MS). Significant decreases in TH and DR1 transcripts and HVA levels, as well as ratios of HVA/dopamine and HVAþDOPAC/dopamine, in zebrafish embryos were observed after bifenthrin treatment. In juveniles, a significant increase in the expression of ERb1 and the DOPAC to dopamine ratio was noted. These results show a possible antiestrogenic effect of bifenthrin in embryos, and estrogenicity in juveniles, indicating life-stage-dependent toxicity in developing fish. Environ Toxicol Chem 2018;37:236-246. C 2017 SETAC

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Multigene Biomarkers of Pyrethroid Exposure: Exploratory Experiments

Kostich

Bencic

Batt

et al. 2019

Enviro Toxic and Chemistry

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We describe initial development of microarray‐based assays for detecting 4 pyrethroid pesticides (bifenthrin, cypermethrin, esfenvalerate, and permethrin) in water. To facilitate comparison of transcriptional responses with gross apical responses, we estimated concentration–mortality curves for these pyrethroids using flow‐through exposures of newly hatched Daphnia magna, Pimephales promelas adults, and 24 h posthatch P. promelas. Median lethal concentration (LC50) estimates were below most reported values, perhaps attributable to the use of flow‐through exposures or of measured rather than nominal concentrations. Microarray analysis of whole P. promelas larvae and brains from exposed P. promelas adults showed that assays using either tissue type can detect these pyrethroids at concentrations below LC50 values reported for between 72 and 96% of aquatic species, depending on the pesticide. These estimates are conservative because they correspond to the lowest concentrations tested. This suggests that the simpler and less expensive whole‐larval assay provides adequate sensitivity for screening contexts where acute aquatic lethality is observed, but the responsible agent is not known. Gene set analysis (GSA) highlighted several Gene Ontology (GO) terms consistent with known pyrethroid action, but the implications of other GO terms are less clear. Exploration of the sensitivity of results to changes in data processing suggests robustness of the detection assay results, but GSA results were sensitive to methodological variations. Environ Toxicol Chem 2019;38:2436–2446. Published 2019 Wiley Periodicals, Inc. on behalf of SETAC. This article is a US government work, and as such, is in the public domain in the United States of America

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Transcriptomic changes underlie altered egg protein production and reduced fecundity in an estuarine model fish exposed to bifenthrin

Cited by 77 publications

References 88 publications

Developmental exposure to environmentally relevant concentrations of bifenthrin alters transcription of mTOR and ryanodine receptor-dependent signaling molecules and impairs predator avoidance behavior across early life stages in inland silversides (Menidia beryllina)

Developmental exposure to environmentally relevant concentrations of bifenthrin alters transcription of mTOR and ryanodine receptor-dependent signaling molecules and impairs predator avoidance behavior across early life stages in inland silversides (Menidia beryllina)

Effects of bifenthrin exposure on the estrogenic and dopaminergic pathways in zebrafish embryos and juveniles

Multigene Biomarkers of Pyrethroid Exposure: Exploratory Experiments

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