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Molecular mechanism of the suppression of larval skeleton by polycyclic aromatic hydrocarbons in early development of sea urchin Hemicentrotus pulcherrimus

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Abstract

Polycyclic aromatic hydrocarbons including benz[a]anthracene (BaA) are priority pollutants in the aquatic environment. Our previous study revealed that BaA and its metabolite, 4-monohydroxylated BaA (4-OHBaA) inhibit larval skeletogenesis in the sea urchin Hemicentrotus pulcherrimus. Here we report studies to elucidate the target of skeletogenesis inhibition elicited by BaA and 4-OHBaA. First, we performed an in vitro experiment using isolated micromeres which give rise to the larval skeletogenic mesenchyme. However, skeletogenesis was not repressed by BaA and 4-OHBaA, implying that these chemicals indirectly influence on the formation of larval skeleton. Next, we analyzed their influence in vivo using embryos. Vascular endothelial growth factor (VEGF) that is expressed in the ectoderm and induces spicule formation was inhibited by BaA and 4-OHBaA treatment. These chemicals also suppressed the expression of the heparan sulfate 6-O endosulfatase (Sulf) known as a VEGF signaling modulator. We, therefore, propose that BaA and 4-OHBaA effects on larval skeletogenesis via VEGF signaling. Furthermore, we showed that the expression of Endo16 mRNA, an endodermal marker, decreased after BaA and 4-OHBaA exposure, suggesting that these chemicals affect endodermal function together with skeletogenesis. This study demonstrates that BaA and 4-OHBaA exert multiple detrimental effects on the development of H. pulcherrimus.

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Acknowledgements

This research was supported by grant to T.S., K.H., and N.S. (Program for Advancing Strategic International Networks to Accelerate the Circulation of Talented Researchers no. G2702 by JSPS). Grants to T. S. (Scientific Research [C] no. 18K06312 by JSPS) and to N.S. (Grant-in-Aid for Scientific Research [C] no. 16K07871 by JSPS) partially support this investigation. This study was conducted as part of the cooperative research program of Institute of Nature and Environmental Technology, Kanazawa University <Accept no. 17021>.

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Correspondence to Nobuo Suzuki.

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Sekiguchi, T., Yachiguchi, K., Kiyomoto, M. et al. Molecular mechanism of the suppression of larval skeleton by polycyclic aromatic hydrocarbons in early development of sea urchin Hemicentrotus pulcherrimus. Fish Sci 84, 1073–1079 (2018). https://doi.org/10.1007/s12562-018-1245-y

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  • DOI: https://doi.org/10.1007/s12562-018-1245-y

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