Early Life Exposure to Environmentally Relevant Levels of Endocrine Disruptors Drive Multigenerational and Transgenerational Epigenetic Changes in a Fish Model

Major, Kaley M.; DeCourten, Bethany M.; Li, Jie; Britton, Monica; Settles, Matthew L.; Mehinto, Alvine C.; Connon, Richard E.; Brander, Susanne M.

doi:10.3389/fmars.2020.00471

Cited by 36 publications

(27 citation statements)

References 98 publications

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“…Moreover, differential methylation of 17b-hsd and ar was found across generations (163). A similar study on the same species exposed to EE2 up to 21 dph, revealed changes in biological processes and pathways involved in growth, development and reproduction as assessed by GO and pathway analyses, and methylation of hormone receptors, steroidogenesis, and sexual development-related genes across generations (164). In fathead minnow, BPA inhibited body length and body weight in F0 males after up to 164 days of exposure.…”

Section: Sub-chronic/chronic Exposurementioning

confidence: 63%

Experimental Approaches for Characterizing the Endocrine-Disrupting Effects of Environmental Chemicals in Fish

2021

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Increasing industrial and agricultural activities have led to a disturbing increase of pollutant discharges into the environment. Most of these pollutants can induce short-term, sustained or delayed impacts on developmental, physiological, and behavioral processes that are often regulated by the endocrine system in vertebrates, including fish, thus they are termed endocrine-disrupting chemicals (EDCs). Physiological impacts resulting from the exposure of these vertebrates to EDCs include abnormalities in growth and reproductive development, as many of the prevalent chemicals are capable of binding the receptors to sex steroid hormones. The approaches employed to investigate the action and impact of EDCs is largely dependent on the specific life history and habitat of each species, and the type of chemical that organisms are exposed to. Aquatic vertebrates, such as fish, are among the first organisms to be affected by waterborne EDCs, an attribute that has justified their wide-spread use as sentinel species. Many fish species are exposed to these chemicals in the wild, for either short or prolonged periods as larvae, adults, or both, thus, studies are typically designed to focus on either acute or chronic exposure at distinct developmental stages. The aim of this review is to provide an overview of the approaches and experimental methods commonly used to characterize the effects of some of the environmentally prevalent and emerging EDCs, including 17 α-ethinylestradiol, nonylphenol, BPA, phthalates, and arsenic; and the pervasive and potential carriers of EDCs, microplastics, on reproduction and growth. In vivo and in vitro studies are designed and employed to elucidate the direct effects of EDCs at the organismal and cellular levels, respectively. In silico approaches, on the other hand, comprise computational methods that have been more recently applied with the potential to replace extensive in vitro screening of EDCs. These approaches are discussed in light of model species, age and duration of EDC exposure.

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Section: Sub-chronic/chronic Exposurementioning

confidence: 63%

Experimental Approaches for Characterizing the Endocrine-Disrupting Effects of Environmental Chemicals in Fish

2021

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“…Future studies will address this issue by sequencing the whole epigenome of the brain and testicular somatic cells affected by ancestral BPA and EE2 exposure. In inland silverside, Menidia beryllina, whole body epigenome and transcriptome analyses revealed significant differences in the promoter and/or gene body methylation in EE2-exposed fish relative to controls and all generations (F0-F2), indicating an association of inheritance of DNA methylation alterations with both multigenerational (F1) and transgenerational (F2) effects that were observed [69]. In zebrafish, epigenetic alterations are associated with gonad homeostasis [70] and sexual development [71].…”

Section: Discussionmentioning

confidence: 94%

Bisphenol A and 17α-ethinylestradiol-induced transgenerational gene expression differences in the brain–pituitary–testis axis of medaka, Oryzias latipes†

Thayil

Wang

Bhandari

et al. 2020

Biology of Reproduction

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Endocrine disrupting chemicals (EDCs), such as Bisphenol A (BPA) and 17α-ethinylestradiol (EE2), can have far reaching health effects, including transgenerational abnormalities in offspring that never directly contacted either chemical. We previously reported reduced fertilization rates and embryo survival at F2 and F3 generations caused by 7-day embryonic exposure (F0) to 100 μg/L BPA or 0.05 μg/L EE2 in medaka. Crossbreeding of fish in F2 generation indicated subfertility in males. To further understand the mechanisms underlying BPA or EE2-induced adult onset and transgenerational reproductive defects in males, the present study examined the expression of genes regulating the brain-pituitary-testis (BPT) axis in the same F0 and F2 generation male medaka. Embryonic exposure to BPA or EE2 led to hyperactivation of brain and pituitary genes which are actively involved in reproduction in adulthood of the F0 generation male fish, and some of these F0 effects continued to the F2 generation (transgenerational effects). Particularly, the F2 generation inherited the hyperactivated state of expression for kisspeptin (kiss1 and kiss2) and their receptors (kiss1r and kiss2r), and gnrh and gnrh receptors. At F2 generation expression of DNA methyltransferase 1 (dnmt1) decreased in brain of the BPA treatment lineage, while EE2 treatment lineage showed increased dnmt3bb expression. Global hypomethylation pattern was observed in the testis of both F0 and F2 generation fish. Taken together, these results demonstrated that BPA or EE2-induced transgenerational reproductive impairment in the F2 generation was associated with alterations of reproductive genes expression in brain and testis and global DNA methylation in testis.

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“…DNA concentration was adjusted to 0.65 ng/µl and loaded onto a Chromium Genome Chip. Libraries were prepared using the Chromium Genome Library & Gel Bead Kit v.2 (10× Genomics) and Chromium controller according to manufacturer’s recommendations, but with additional shearing ( Major et al 2020 ). The library was quantified by qPCR using a Kapa Library Quantification Kit (Kapa Biosystems-Roche) and sequenced on a partial lane of NovaSeq6000 (Illumina, San Diego, CA) with paired-end 150 bp reads.…”

Section: Methodsmentioning

confidence: 99%

De Novo Whole-Genome Assembly of the Swede Midge (Contarinia nasturtii), a Specialist of Brassicaceae, Using Linked-Read Sequencing

Mori

Coutu

Chen

et al. 2021

Genome Biology and Evolution

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The swede midge, Contarinia nasturtii, is a cecidomyiid fly that feeds specifically on plants within the Brassicaceae. Plants in this family employ a glucosinolate-myrosinase defense system, which can be highly toxic to non-specialist feeders. Feeding by C. nasturtii larvae induces gall formation, which can cause substantial yield losses thus making it a significant agricultural pest. A lack of genomic resources, in particular a reference genome, has limited deciphering the mechanisms underlying glucosinolate tolerance in C. nasturtii, which is of particular importance for managing this species. Here, we present an annotated, scaffolded reference genome of C. nasturtii using linked-read sequencing from a single individual and explore systems involved in glucosinolate detoxification. The C. nasturtii genome is similar in size and annotation completeness to that of the Hessian fly, Mayetiola destructor, but has greater contiguity. Several genes encoding enzymes involved in glucosinolate detoxification in other insect pests, including myrosinases, sulfatases, and glutathione S-transferases, were found, suggesting that C. nasturtii has developed similar strategies for feeding on Brassicaceae. The C. nasturtii genome will, therefore, be integral to continued research on plant-insect interactions in this system and contribute to effective pest management strategies.

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Early Life Exposure to Environmentally Relevant Levels of Endocrine Disruptors Drive Multigenerational and Transgenerational Epigenetic Changes in a Fish Model

Cited by 36 publications

References 98 publications

Experimental Approaches for Characterizing the Endocrine-Disrupting Effects of Environmental Chemicals in Fish

Experimental Approaches for Characterizing the Endocrine-Disrupting Effects of Environmental Chemicals in Fish

Bisphenol A and 17α-ethinylestradiol-induced transgenerational gene expression differences in the brain–pituitary–testis axis of medaka, Oryzias latipes†

De Novo Whole-Genome Assembly of the Swede Midge (Contarinia nasturtii), a Specialist of Brassicaceae, Using Linked-Read Sequencing

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