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Zoomorphology

, Volume 138, Issue 1, pp 117–126 | Cite as

The ontogeny of synaptophysin expression patterns on the GABAergic ciliary band-associated strand during larval development of the sea urchin, Hemicentrotus pulcherrimus A. Agassiz, 1864

  • Hideki KatowEmail author
  • Tomoko Katow
  • Masato Kiyomoto
Original paper
  • 72 Downloads

Abstract

The swimming activity of sea urchin larvae depends on the ciliary beating primarily generated at the circumoral ciliary band (CB) and is regulated by several neurotransmitters, including γ-aminobutyric acid (GABA). Although GABA is primarily localized in the CB, its synthetase glutamate decarboxylase (GAD) is not expressed in the CB but in the ciliary band-associated strand (CBAS). The CBAS expresses synaptophysin (Syp), a major synaptic vesicle component that is detected in the GAD-expressing puncta. In this study, we analyzed the ontogeny of the spatiotemporal expression pattern of Syp. Syp was initially detected in the cytoplasm of small patches of ectodermal cells from the mesenchyme blastula stage, then along with GABA from the mid-gastrula stage. At the prism stage, the blastocoelar cells also expressed Syp and GABA. In larvae, GABA was detected in the CBAS and the CB. The latter also expressed the GABA(A) receptor. A GAD inhibitor, 3-mercaptopropionic acid, inhibited GABA expression in the CBAS and the CB. During and after the 4-arm pluteus stage (4aPL), the CBAS completed the encircling of the oral ectoderm region, which, however, left the CBAS-absent upper oral lobe region. The present study indicated close localization of GABA and Syp in the puncta of the CBAS and that of GABA and GABA(A)R in the CB, and that, for the first time in the sea urchin nervous system, implicates the Syp-mediated efferent GABA transmission from the CBAS to the CB.

Keywords

GABAergic regulation Synaptic transmission 3-MPA Ciliary band Immunohistochemistry 

Abbreviations

Ab

Antibody

AmT

Ambient temperature

CB

The ciliary band

CBAS

The ciliary band-associated strand

CLSM

Confocal laser-scanning microscope

EV

Endoplasmic vesicles

FSW

Filtered sea water

GABA

Gamma-amino butyric acid

GABA(A)R

GABA(A) receptor

GABARAP

GABA(A)R-associated protein

GAD

Glutamate decarboxylase

IB

Immunoblotting

IS

Immunopositive signal

mBL

Mesenchyme blastula

PBST

0.1 M phosphate-buffered saline with Tween-20

sBL

Swimming blastula

Syp

Synaptophysin

SV

Synaptic vesicle

WMIHC

Whole-mount immunohistochemistry

1/2G

Gastrulation half-completed gastrula

3D

Three dimensional

3-MPA

3-Mercaptopropionic acid

4aPL

4-Arm pluteus larva

6aPL

6-Arm pluteus larva

8aPL

8-Arm pluteus larva

Notes

Acknowledgements

We thank Ms. Hiromi Yoshida (Tohoku University, Japan) for technical support for the 3D reconstructions.

Funding

This study was partly supported by the Cooperative Research Project Program of the Joint Usage/Research Center at the Institute of Development, Aging and Cancer, Tohoku University (No. 5, 2016).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Data availability

All data generated or analyzed during this study are included in this published article.

Informed consent

On behalf of my co-authors, I declare that the manuscript has not been published elsewhere and has not been submitted to any other journal.

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Research Center for Marine BiologyTohoku UniversityAomoriJapan
  2. 2.Institute of Development, Aging and CancerTohoku UniversitySendaiJapan
  3. 3.Marine and Coastal Research CenterOchanomizu UniversityChibaJapan

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