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Larval arm resorption proceeds concomitantly with programmed cell death during metamorphosis of the sea urchin Hemicentrotus pulcherrimus

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Abstract

Sea urchins are excellent models to elucidate metamorphic phenomena of echinoderms. However, little attention has been paid to the way that their organ resorption is accomplished by programmed cell death (PCD) and related cellular processes. We have used cytohistochemistry and transmission electron microscopy to study arm resorption in competent larvae of metamorphosing sea urchins, Hemicentrotus pulcherrimus, induced to metamorphose by L-glutamine treatment. The results show that: (1) columnar epithelial cells, which are constituents of the ciliary band, undergo PCD in an overlapping fashion with apoptosis and autophagic cell death; (2) squamous epithelial cells, which are distributed between the two arrays of the ciliary band, display a type of PCD distinct from that of columnar epithelial cells, i.e., a cytoplasmic type of non-lysosomal vacuolated cell death; (3) epithelial integrity is preserved even when PCD occurs in constituent cells of the epithelium; (4) secondary mesenchyme cells, probably blastocoelar cells, contribute to the elimination of dying epithelial cells; (5) nerve cells have a delayed initiation of PCD. Taken together, our data indicate that arm resorption in sea urchins proceeds concomitantly with various types of PCD followed by heterophagic elimination, but that epithelial organization is preserved during metamorphosis.

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Acknowledgements

We are grateful to Prof. Yoshinori Ohsumi and Dr. Eiko Oita for their kind suggestions regarding the identification of the morphology of autophagic vacuoles, to Profs. Kiyoaki Kuwasawa and Shinichi Hisanaga for their valuable discussions, and to Dr. Isao Uemura for his technical advice on electron microscopy. We are indebted to members of the Marine and Coastal Research Center of Ochanomizu University and to Profs. Takashi Suyemitsu and Masato Kiyomoto, Ms. Mamiko Yajima and Ms. Ayumi Kikuchi for supplying sea urchin larvae. Our thanks are also due to Dr. Masashi Noguchi for his useful suggestions and for supplying larvae.

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Authors and Affiliations

  1. Department of Biology, Keio University, Hiyoshi 4-1-1, Kohoku-ku, Yokohama, 223-8521, Japan

    Yukiko Sato, Hiroyuki Kaneko & Sumiko Negishi

  2. Department of Biology, Faculty of Science, Tokyo Metropolitan University, Minamiosawa, Hachioji, Tokyo, 192-0397, Japan

    Yukiko Sato & Ikuko Yazaki

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  1. Yukiko Sato
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  2. Hiroyuki Kaneko
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  3. Sumiko Negishi
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  4. Ikuko Yazaki
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Correspondence to Yukiko Sato.

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This investigation was supported in part by a Keio University special grant-in-aid for innovative collaborative research projects.

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Sato, Y., Kaneko, H., Negishi, S. et al. Larval arm resorption proceeds concomitantly with programmed cell death during metamorphosis of the sea urchin Hemicentrotus pulcherrimus . Cell Tissue Res 326, 851–860 (2006). https://doi.org/10.1007/s00441-006-0212-6

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