Involvement of Netrin/Unc-5 Interaction in Ciliary Beating and in Pattern Formation of the Ciliary Band-Associated Strand (CBAS) in the Sea Urchin, <i>Hemicentrotus pulcherrimus</i>

The GABAergic neural circuit is involved in the motile activities of both larval and juvenile sea urchins. Therefore, its function is inherited beyond metamorphosis, despite large scale remodeling of larval organs during that period. However, the initial neural circuit formation mechanism is not wel...

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Main Authors: Hideki Katow, Kouki Abe, Tomoko Katow, Hiromi Yoshida, Masato Kiyomoto
Format: Article
Language:English
Published: MDPI AG 2020-09-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/21/18/6587
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author Hideki Katow
Kouki Abe
Tomoko Katow
Hiromi Yoshida
Masato Kiyomoto
author_facet Hideki Katow
Kouki Abe
Tomoko Katow
Hiromi Yoshida
Masato Kiyomoto
author_sort Hideki Katow
collection DOAJ
description The GABAergic neural circuit is involved in the motile activities of both larval and juvenile sea urchins. Therefore, its function is inherited beyond metamorphosis, despite large scale remodeling of larval organs during that period. However, the initial neural circuit formation mechanism is not well understood, including how glutamate decarboxylase-expressing blastocoelar cells (GADCs) construct the neural circuit along the circumoral ciliary band (a ciliary band-associated strand, CBAS) on the larval body surface. In this study, using whole-mount immunohistochemistry and 3D reconstructed imaging, the ontogenic process of CBAS patterning was studied by focusing on Netrin and the interaction with its receptor, Unc-5. During the early 2-arm pluteus stage, a small number of GADCs egress onto the apical surface of the larval ectoderm. Then, they line up on the circumoral side of the ciliary band, and by being inserted by a further number of GADCs, form longer multicellular strands along the Netrin stripe. Application of a synthetic peptide, CRFNMELYKLSGRKSGGVC of Hp-Netrin, that binds to the immunoglobulin domain of Unc-5 during the prism stage, causes stunted CBAS formation due to inhibition of GADC egression. This also results in reduced ciliary beating. Thus, the Netrin/Unc-5 interaction is involved in the construction and function of the CBAS.
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spelling doaj.art-092e1661a15c45ad9701c69cead018882023-11-20T13:03:56ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-09-012118658710.3390/ijms21186587Involvement of Netrin/Unc-5 Interaction in Ciliary Beating and in Pattern Formation of the Ciliary Band-Associated Strand (CBAS) in the Sea Urchin, <i>Hemicentrotus pulcherrimus</i>Hideki Katow0Kouki Abe1Tomoko Katow2Hiromi Yoshida3Masato Kiyomoto4Research Center for Marine Biology, Tohoku University, Asamushi, Aomori 039-3501, JapanResearch Center for Marine Biology, Tohoku University, Asamushi, Aomori 039-3501, JapanResearch Center for Marine Biology, Tohoku University, Asamushi, Aomori 039-3501, JapanInstitute of Development, Aging and Cancer, Tohoku University, Sendai 980-8575, JapanInstitute of Development, Aging and Cancer, Tohoku University, Sendai 980-8575, JapanThe GABAergic neural circuit is involved in the motile activities of both larval and juvenile sea urchins. Therefore, its function is inherited beyond metamorphosis, despite large scale remodeling of larval organs during that period. However, the initial neural circuit formation mechanism is not well understood, including how glutamate decarboxylase-expressing blastocoelar cells (GADCs) construct the neural circuit along the circumoral ciliary band (a ciliary band-associated strand, CBAS) on the larval body surface. In this study, using whole-mount immunohistochemistry and 3D reconstructed imaging, the ontogenic process of CBAS patterning was studied by focusing on Netrin and the interaction with its receptor, Unc-5. During the early 2-arm pluteus stage, a small number of GADCs egress onto the apical surface of the larval ectoderm. Then, they line up on the circumoral side of the ciliary band, and by being inserted by a further number of GADCs, form longer multicellular strands along the Netrin stripe. Application of a synthetic peptide, CRFNMELYKLSGRKSGGVC of Hp-Netrin, that binds to the immunoglobulin domain of Unc-5 during the prism stage, causes stunted CBAS formation due to inhibition of GADC egression. This also results in reduced ciliary beating. Thus, the Netrin/Unc-5 interaction is involved in the construction and function of the CBAS.https://www.mdpi.com/1422-0067/21/18/6587CBASpattern formationNetrin/Unc-5 interaction3D reconstructionsea urchin larva
spellingShingle Hideki Katow
Kouki Abe
Tomoko Katow
Hiromi Yoshida
Masato Kiyomoto
Involvement of Netrin/Unc-5 Interaction in Ciliary Beating and in Pattern Formation of the Ciliary Band-Associated Strand (CBAS) in the Sea Urchin, <i>Hemicentrotus pulcherrimus</i>
International Journal of Molecular Sciences
CBAS
pattern formation
Netrin/Unc-5 interaction
3D reconstruction
sea urchin larva
title Involvement of Netrin/Unc-5 Interaction in Ciliary Beating and in Pattern Formation of the Ciliary Band-Associated Strand (CBAS) in the Sea Urchin, <i>Hemicentrotus pulcherrimus</i>
title_full Involvement of Netrin/Unc-5 Interaction in Ciliary Beating and in Pattern Formation of the Ciliary Band-Associated Strand (CBAS) in the Sea Urchin, <i>Hemicentrotus pulcherrimus</i>
title_fullStr Involvement of Netrin/Unc-5 Interaction in Ciliary Beating and in Pattern Formation of the Ciliary Band-Associated Strand (CBAS) in the Sea Urchin, <i>Hemicentrotus pulcherrimus</i>
title_full_unstemmed Involvement of Netrin/Unc-5 Interaction in Ciliary Beating and in Pattern Formation of the Ciliary Band-Associated Strand (CBAS) in the Sea Urchin, <i>Hemicentrotus pulcherrimus</i>
title_short Involvement of Netrin/Unc-5 Interaction in Ciliary Beating and in Pattern Formation of the Ciliary Band-Associated Strand (CBAS) in the Sea Urchin, <i>Hemicentrotus pulcherrimus</i>
title_sort involvement of netrin unc 5 interaction in ciliary beating and in pattern formation of the ciliary band associated strand cbas in the sea urchin i hemicentrotus pulcherrimus i
topic CBAS
pattern formation
Netrin/Unc-5 interaction
3D reconstruction
sea urchin larva
url https://www.mdpi.com/1422-0067/21/18/6587
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