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Exogastrulation and interference with the expression of major yolk protein by estrogens administered to sea urchins

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Abstract

Although estrogens have been detected in some echinoderm species, their role is not clearly understood; so we examined the effects of estrogens administered to sea urchin embryos and larvae. A typical malformation was exogastrulation, induced by the exposure to ethynylestradiol (EER) in a defined period of 12 h from 12 h after fertilization (HAF). Morphogenesis for gastrulation was delayed in the treated embryos: protrusion of the archenteron started at 30 HAF when gastrulation had already finished in normal embryos. Exogastrulation induced by EER was cancelled by the antiestrogen chemical, ICI182,780. Feeding larvae were less sensitive to estrogens than those in early embryogenesis and, at certain concentrations, developed without abnormal morphology. The effect of estrogens was examined at the level of gene expression of the major yolk protein (MYP). MYP expression started during the larval stage and was suppressed by estrone at the six-armed stage, but not by β-estradiol, and in later stage larvae, the expression was not affected by treatment with either estrogen. Estrogens affect sea urchins in the early stage of embryogenesis, leading to abnormal morphogenesis and interference with gene expression.

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Abbreviations

DAF:

days after fertilization

EER:

ethynylestradiol

HAF:

hours after fertilization

ICI:

ICI182,780

MYP:

major yolk protein

RT-PCR:

reverse transcription polymerase chain reaction

TAM:

tamoxifen

References

  • Cervello M, Matranga V. Evidence of a precursor–product relationship between vitellogenin and toposome, a glycoprotein complex mediating cell adhesion. Cell Differ Dev 1989;26:67–76.

    Article  PubMed  CAS  Google Scholar 

  • Dan K, Okazaki K. Cyto-embryological studies of sea urchins. III. Role of the secondary mesenchyme cells in the formation of the primitive gut in sea urchin larvae. Biol Bull 1956;110:29–42.

    Article  Google Scholar 

  • Harrington FL, Ozaki H. The effect of estrogen on protein synthesis in echinoid coelomocytes. Comp Biochem Physiol 1986;84B:417–21.

    CAS  Google Scholar 

  • Hayley M, Perera A, Robinson JJ. Biochemical analysis of a Ca2+-dependent membrane–membrane interaction mediated by the sea urchin yolk granule protein, toposome. Dev Growth Differ 2006;48:401–9.

    Article  PubMed  CAS  Google Scholar 

  • Hiramatsu N, Matsubara T, Fujita T, Sullivan CV, Hara A. Multiple piscine vitellogenins: biomarkers of fish exposure to estrogenic endocrine disruptors in aquatic environments. Mar Biol 2006;149:35–47.

    Article  CAS  Google Scholar 

  • Hirate Y, Tomita K, Yamamoto S, Kobari K, Uemura I, Yamasu K, Suyemitsu T. Association of the sea urchin EGF-related peptide, EGIP-D, with fasciclin I-related ECM proteins from the sea urchin Anthocidaris crassispina. Dev Growth Differ 1999;41:483–94.

    Article  PubMed  CAS  Google Scholar 

  • Ishihara K, Tonegawa Y, Suyemitsu T, Kubo H. The blastocoelic fluid of sea urchin embryo induces exogastrulation. J Exp Zool 1982;220:227–33.

    Article  CAS  Google Scholar 

  • Kiyomoto M, Kikuchi A, Unuma T, Yokota Y. Effects of ethynylestradiol and bisphenol a on the development of sea urchin embryos and juveniles. Mar Biol 2006;149:57–63.

    Article  CAS  Google Scholar 

  • Kominami T, Takata H. Gastrulation in the sea urchin embryo: a model system for analyzing the morphogenesis of a monolayered epithelium. Dev Growth Differ 2004;46:309–26.

    Article  PubMed  Google Scholar 

  • Komukai M, Iizuka Y, Yasumasu I. Synthesis of protein enriched in Li+-induced vegetalized embryos of sea urchin during early development. Dev Growth Differ 1989;31:371–8.

    Article  CAS  Google Scholar 

  • Livingston BT, Wilt FH. Lithium evokes expression of vegetal-specific molecules in the animal blastomeres of sea urchin embryos. Proc Natl Acad Sci U S A 1989;86:3669–73.

    Article  PubMed  CAS  Google Scholar 

  • Logan CY, Miller JR, Ferkowiez MJ, McClay DR. Nuclear b-catenin is required to specify vegetal cell fates in the sea urchin embryo. Development 1999;126:345–57.

    PubMed  CAS  Google Scholar 

  • Mwatibo JM, Green JD. Estradiol disrupts sea urchin embryogenesis differently from methoxychlor. Bull Environ Contam Toxicol 1998;61:577–82.

    Article  PubMed  CAS  Google Scholar 

  • Noll H, Matranga V, Cervello M, Humphreys T, Kuwasaki B, Adelson D. Characterization of toposomes from sea urchin blastula cells: a cell organelle mediating cell adhesion and expressing positional information. Proc Natl Acad Sci U S A 1985;82:8062–6.

    Article  PubMed  CAS  Google Scholar 

  • Noll H, Alcedo J, Daube M, Frei E, Schiltz E, Humpries T, Matranga V, Hochstrasser M, Aebersold R, Lee H, Noll M. The toposome, essential for sea urchin cell adhesion and development, is a modified iron-less calcium-binding transferin. Dev Biol 2007;310:54–70.

    Article  PubMed  CAS  Google Scholar 

  • Okazaki K. Exogastrulation induced by calcium deficiency in the sea urchin, Pseudocentrotus depressus. Embryologia 1956;3:23–36.

    Article  Google Scholar 

  • Oetken M, Bachmann J, Schulte-Oehlmann U, Oehlmann J. Evidence for endocrine disruption in invertebrates. Int Rev Cytol 2004;236:1–44.

    Article  PubMed  CAS  Google Scholar 

  • Pillai MC, Vines CA, Wikramanayake AH, Cherr GN. Polycyclic aromatic hydrocarbons disrupt axial development in sea urchin embryos through a b-catenin dependent pathway. Toxicology 2003;186:93–108.

    Article  PubMed  CAS  Google Scholar 

  • Roepke TA, Synder MJ, Cherr GN. Estradiol and endocrine disrupting compounds adversely affect development of sea urchin embryos at environmentally relevant concentrations. Aquat Toxicol 2005;71:155–73.

    Article  PubMed  CAS  Google Scholar 

  • Schoenmakers HJN, Dieleman SJ. Progesterone and estrone levels in the ovaries, pyloric ceca, and perivisceral fluid during the annual reproductive cycle of the starfish, Asterias rubens. Gen Comp Endocrinol 1981;43:63–70.

    Article  PubMed  CAS  Google Scholar 

  • Scott LB, Leahy PS, Decker GL, Lennarz WJ. Loss of yolk platelets and yolk glycoproteins during larval development of the sea urchin embryo. Dev Biol 1990;137:368–77.

    Article  PubMed  CAS  Google Scholar 

  • Shyu AB, Raff RA, Blumenthal T. Expression of the vitellogenin gene in female and male sea urchin. Proc Natl Acad Sci U S A 1986;83:3865–9.

    Article  PubMed  CAS  Google Scholar 

  • Shyu AB, Blumenthal T, Raff RA. A single gene encoding vitellogenin in the sea urchin Strongylocentrotus purpuratus: sequence at the 5′ end. Nucleic Acids Res 1987;15:10405–17.

    Article  PubMed  CAS  Google Scholar 

  • Sugni M, Mozzi D, Barbaglio A, Bonasoro F, Candia Carnevali MD. Endocrine disrupting compounds and echinoderms: new ecotoxicological sentinels for the marine ecosystem. Ecotoxicology 2007;16:95–108.

    Article  PubMed  CAS  Google Scholar 

  • Suyemitsu T, Asami-Yoshizumi T, Noguchi S, Tonegawa Y, Ishihara K. The exogastrula-inducing peptides in embryos of the sea urchin, Anthocidaris crassispina: isolation and determination of the primary structure. Cell Differ Dev 1989;26:53–66.

    Article  PubMed  CAS  Google Scholar 

  • Takata H, Kominami T. Shrinkage and expansion of blastocoel affect the degree of invagination in sea urchin embryos. Zoological Science 2001;18:1097–105.

    Article  Google Scholar 

  • Unuma T, Yamamoto T, Akiyama T. Effects of oral administration of steroids on the growth of juvenile sea urchin Pseudocentrotus depressus. Suisanzoshoku 1996;44:79–83. (in Japanese with English abstract).

    CAS  Google Scholar 

  • Unuma T, Suzuki T, Kurokawa T, Yamamoto T, Akiyama T. A protein identical to the yolk protein is stored in the testis in male sea urchin, Pseudocentrotus depressus. Biol Bull 1998;194:92–7.

    Article  CAS  Google Scholar 

  • Unuma T, Yamamoto T, Akiyama T. Effects of steroids on gonadal growth and gametogenesis in the juvenile red sea urchin Pseudocentrotus depressus. Biol Bull 1999;196:199–204.

    Article  CAS  Google Scholar 

  • Unuma T, Okamoto H, Konishi K, Ohta H, Mori K. Cloning of cDNA encoding vitellogenin and its expression in red sea urchin, Pseudocentrotus depressus. Zoological Science 2001;18:559–65.

    Article  CAS  Google Scholar 

  • Unuma T, Yamamoto T, Akiyama T, Shiraishi M, Ohta H. Quantitative changes in yolk protein and other components in the ovary and testis of the sea urchin Pseudocentrotus depressus. J Exp Biol 2003;206:365–72.

    Article  PubMed  CAS  Google Scholar 

  • Unuma T, Ikeda K, Yamano K, Moriyama A, Ohta H. Zinc-binding property of the major yolk protein in the sea urchin: implications of its role as a zinc transporter for gametogenesis. FEBS J 2007;274:4985–98.

    Article  PubMed  CAS  Google Scholar 

  • Wasson KM, Gower BA, Hines GA, Watts SA. Levels of progesterone, testosterone, and estradiol and the androstenedione metabolism in the gonads of Lytechinus variegatus (Echinodermata: Echinoidea). Comp Biochem Physiol 2000a;126C:153–65.

    CAS  Google Scholar 

  • Wasson KM, Gower BA, Watts SA. Responses of ovaries and testes of Lytechinus variegatus (Echinodermata: Echinoidea) to dietary administration of estradiol, progesterone and testosterone. Mar Biol 2000b;137:245–55.

    Article  CAS  Google Scholar 

  • Wikramanayake AH, Klein WH. Multiple signaling events specify ectoderm and pattern the oral–aboral axis in the sea urchin embryo. Development 1997;124:13–20.

    PubMed  CAS  Google Scholar 

  • Wikramanayake AH, Huang L, Klein WH. Catenin is essential for patterning the maternally specified animal–vegetal axis in the sea urchin embryo. Proc Natl Acad Sci U S A 1998;95:9343–48.

    Article  PubMed  CAS  Google Scholar 

  • Xu RA, Barker MF. Annual changes in the steroid levels in the ovaries and the pyloric caeca of Sclerasterias mollis (Echinodermata: Asteroidea) during the reproductive cycle. Comp Biochem Physiol 1990;95A:127–34.

    Article  CAS  Google Scholar 

  • Yamasu K, Watanabe H, Kohchi C, Soma G, Mizuno D, Akasaka K, Shimada H, Suyemitsu T, Ishihara K. Molecular cloning of a cDNA that encodes the precursor to several exogastrula-inducing peptides, epidermal-growth-factor-related polypeptides of the sea urchin Anthocidaris crassispina. Eur J Biochem 1995;228:515–23.

    Article  PubMed  CAS  Google Scholar 

  • Yokota Y, Sappington TW. Vitellogen and vitellogenin in echinoderms. In: Raikhel AS, Sappington TW, editors. Progress in vitellogenesis, reproductive biology of invertebrates, vol. XII, pt A. Enfield: Science; 2002. p. 201–21.

    Google Scholar 

  • Yokota Y, Unuma T, Moriyama A, Yamano K. Cleavage site of a major yolk protein (MYP) determined by cDNA isolation and amino acid sequencing in sea urchin, Hemicentrotus pulcherrimus. Comp Biochem Physiol 2003;135B:71–81.

    CAS  Google Scholar 

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Acknowledgements

We thank Mr. Mamoru Yamaguchi (Tateyama Marine Laboratory, Marine and Coastal Research Center, Ochanomizu University) and the staff of the International Coastal Research Center, Ocean Research Institute, The University of Tokyo for the animal collections. The study was partly supported through a grant of Long-range Research Initiative (LRI) of the Japan Chemical Industry Association (JCIA).

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Correspondence to Masato Kiyomoto.

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Kiyomoto, M., Kikuchi, A., Morinaga, S. et al. Exogastrulation and interference with the expression of major yolk protein by estrogens administered to sea urchins. Cell Biol Toxicol 24, 611–620 (2008). https://doi.org/10.1007/s10565-008-9073-y

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  • DOI: https://doi.org/10.1007/s10565-008-9073-y

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