Parental exposure to bisphenol A affects pharyngeal cartilage development and causes global transcriptomic changes in zebrafish (Danio rerio) offspring

Huang, Wenlong; Zheng, Shukai; Xiao, Jiefeng; Liu, Caixia; Du, Taifeng; Wu, Kusheng

doi:10.1016/j.chemosphere.2020.126537

Cited by 34 publications

(8 citation statements)

References 62 publications

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“…After BPA exposure, the TGF β signaling and heart tube morphogenesis pathways that were related to heart development were significantly influenced. The results could be supported by the studies that observed the cardiovascular response and heart function following the exposure to BPA in zebrafish . Moreover, during zebrafish embryonic development, part of neural crest cells that are differentiated into parasympathetic neurons can migrate into and intermingle with the myocardium, adopting a myocardial cell lineage .…”

Section: Discussionmentioning

confidence: 52%

“…The results could be supported by the studies that observed the cardiovascular response and heart function following the exposure to BPA in zebrafish. 52 Moreover, during zebrafish embryonic development, part of neural crest cells that are differentiated into parasympathetic neurons can migrate into and intermingle with the myocardium, adopting a myocardial cell lineage. 53 It is reported that the absence of parasympathetic innervation can influence heart rate.…”

Section: Discussionmentioning

confidence: 99%

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Single-Cell Sequencing Reveals Heterogeneity Effects of Bisphenol A on Zebrafish Embryonic Development

Chen

Wang

et al. 2020

Environ. Sci. Technol.

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The embryonic period is a sensitive window for bisphenol A (BPA) exposure. However, embryonic development is a highly dynamic process with changing cell populations. The heterogeneity effects of BPA on fish embryo cells during development remain unclear. We applied single-cell RNA sequencing to analyze the impact of BPA exposure on transcriptome heterogeneity of 64 683 cells from zebrafish embryos at 8, 12, and 30 h postfertilization (hpf). Thirty-eight cell populations were identified and gene expression profiles of 16 cell populations were significantly altered by BPA. At 8 hpf, BPA mainly influenced the outer layer cell populations of embryos, such as neural plate border and enveloping layer cells. At 12 and 30 hpf, nervous system formation and heart morphogenesis were disturbed. The altered differential processes of the neural plate border, neural crest, and neuronal cells were found to lead to increased neurogenesis in zebrafish larvae. In the forebrain, midbrain, neurons, and optic cells, pathways related to cell division and DNA replication and repair were altered. Moreover, BPA also changed transforming growth factor (TGF) β signaling and heart tube morphogenesis in heart cells, leading to a decreased heartbeat in zebrafish larvae. Our study provides a comprehensive understanding of BPA toxicity on fish embryonic development at a single-cell level.

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Section: Discussionmentioning

confidence: 52%

Section: Discussionmentioning

confidence: 99%

Single-Cell Sequencing Reveals Heterogeneity Effects of Bisphenol A on Zebrafish Embryonic Development

Chen

Wang

et al. 2020

Environ. Sci. Technol.

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“…It should be noted that the concentrations used in these studies exceed environmental concentrations. In zebrafish larvae, BPA induced craniofacial malformations by disrupting chondrocyte organization in the pharyngeal structures and inducing apoptosis ( Huang et al, 2020 ). The BPA-based polymer Bis-GMA used in dental fillers decreased palatoquadral length in zebrafish larvae at 10 nM, while the palatoquadral-ceratohyal angle was decreased at 1 μM ( Kramer et al, 2016 ).…”

Section: Estrogens and Craniofacial Malformationsmentioning

confidence: 99%

Zebrafish Models of Craniofacial Malformations: Interactions of Environmental Factors

Raterman

Metz

Wagener

et al. 2020

Front. Cell Dev. Biol.

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The zebrafish is an appealing model organism for investigating the genetic (G) and environmental (E) factors, as well as their interactions (GxE), which contribute to craniofacial malformations. Here, we review zebrafish studies on environmental factors involved in the etiology of craniofacial malformations in humans including maternal smoking, alcohol consumption, nutrition and drug use. As an example, we focus on the (cleft) palate, for which the zebrafish ethmoid plate is a good model. This review highlights the importance of investigating ExE interactions and discusses the variable effects of exposure to environmental factors on craniofacial development depending on dosage, exposure time and developmental stage. Zebrafish also promise to be a good tool to study novel craniofacial teratogens and toxin mixtures. Lastly, we discuss the handful of studies on gene–alcohol interactions using mutant sensitivity screens and reverse genetic techniques. We expect that studies addressing complex interactions (ExE and GxE) in craniofacial malformations will increase in the coming years. These are likely to uncover currently unknown mechanisms with implications for the prevention of craniofacial malformations. The zebrafish appears to be an excellent complementary model with high translational value to study these complex interactions.

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“…APAP is one of only a few compounds examined that significantly disrupts the formation of viscerocranial cartilages in zebrafish, at least at the concentrations tested. Most compounds affecting craniofacial cartilage development result in a reduction in cartilage sizes and/or orientation, such as ethanol [ 46 ], dioxin [ 47 ], valproic acid [ 48 ], bisphenol A [ 49 ], bis-GMA [ 50 ], 6-OH-BDE-47 [ 51 ], perchlorate [ 52 ], atrazine [ 53 ], and several triazole and dithiocarbamate fungicides [ 54 ]. However, craniofacial cartilages are often missing in embryos treated with paclobutrazol [ 55 ], di-butyl phthalate [ 56 ], estradiol [ 57 ], and offspring of female fish exposed to topiramate [ 58 ], with the viscerocranial cartilages primarily affected.…”

Section: Discussionmentioning

confidence: 99%

Acetaminophen Disrupts the Development of Pharyngeal Arch-Derived Cartilage and Muscle in Zebrafish

Glasco

Wang

Kang

et al. 2022

JDB

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Acetaminophen is a common analgesic, but its potential effects on early embryonic development are not well understood. Previous studies using zebrafish (Danio rerio) have described the effects of acetaminophen on liver development and physiology, and a few have described gross physiological and morphological defects. Using a high but non-embryonic lethal dose of acetaminophen, we probed for defects in zebrafish craniofacial cartilage development. Strikingly, acetaminophen treatment caused severe craniofacial cartilage defects, primarily affecting both the presence and morphology of pharyngeal arch-derived cartilages of the viscerocranium. Delaying acetaminophen treatment restored developing cartilages in an order correlated with their corresponding pharyngeal arches, suggesting that acetaminophen may target pharyngeal arch development. Craniofacial cartilages are derived from cranial neural crest cells; however, many neural crest cells were still seen along their expected migration paths, and most remaining cartilage precursors expressed the neural crest markers sox9a and sox10, then eventually col2a1 (type II collagen). Therefore, the defects are not primarily due to an early breakdown of neural crest or cartilage differentiation. Instead, apoptosis is increased around the developing pharyngeal arches prior to chondrogenesis, further suggesting that acetaminophen may target pharyngeal arch development. Many craniofacial muscles, which develop in close proximity to the affected cartilages, were also absent in treated larvae. Taken together, these results suggest that high amounts of acetaminophen can disrupt multiple aspects of craniofacial development in zebrafish.

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Parental exposure to bisphenol A affects pharyngeal cartilage development and causes global transcriptomic changes in zebrafish (Danio rerio) offspring

Cited by 34 publications

References 62 publications

Single-Cell Sequencing Reveals Heterogeneity Effects of Bisphenol A on Zebrafish Embryonic Development

Single-Cell Sequencing Reveals Heterogeneity Effects of Bisphenol A on Zebrafish Embryonic Development

Zebrafish Models of Craniofacial Malformations: Interactions of Environmental Factors

Acetaminophen Disrupts the Development of Pharyngeal Arch-Derived Cartilage and Muscle in Zebrafish

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