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.
GABAergic regulation Synaptic transmission 3-MPA Ciliary band Immunohistochemistry
The ciliary band
The ciliary band-associated strand
Confocal laser-scanning microscope
Filtered sea water
Gamma-amino butyric acid
0.1 M phosphate-buffered saline with Tween-20
Gastrulation half-completed gastrula
4-Arm pluteus larva
6-Arm pluteus larva
8-Arm pluteus larva
This is a preview of subscription content, log in to check access.
We thank Ms. Hiromi Yoshida (Tohoku University, Japan) for technical support for the 3D reconstructions.
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.
All data generated or analyzed during this study are included in this published article.
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.
Bergmann M, Lahr G, Mayerhofer A, Gratzl M (1991) Expression of synaptophysin during the prenatal development of the rat spinal cord: Correlation with basic differentiation processes of neurons. Neuroscience 42:569–582CrossRefGoogle Scholar
Erdö SL, Somogyi J, Hámori J, Amenta F (1986) Light- and electron-microscopic visualization of gamma-aminobutyric acid and GABA-transaminase in the oviduct of rats. Predominant occurrence in epithelium. Cell Tissue Res 244:621–662CrossRefGoogle Scholar
Fletcher TL, Cameron P, De Camilli P, Banker G (1991) The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture. J Neurosci 11:1617–1626CrossRefGoogle Scholar
Mansuy V, Boireau W, Fraichard A, Schlick JL, Jouvenot M, Delage-Mourroux R (2004) GEC1, a protein related to GABARAP, interacts with tubulin and GABA(A) receptor. Biochem Biophys Res Commun 10:639–648CrossRefGoogle Scholar
McMahon HT, Bolshakov VY, Janz R, Hammer RE, Siegelbaum SA, Südhof TC (1996) Synaptophysin, a major synaptic vesicle protein, is not essential for neurotransmitter release. Proc Natl Acad Sci USA 93:4760–4764CrossRefGoogle Scholar
van der Heyden JA, Korf J (1978) Regional levels of GABA in the brain: rapid semiautomated assay and prevention of postmortem increase by 3-mercapto-propionic acid. J Neurochem 31:197–203CrossRefGoogle Scholar
Wang H, Olsen RW (2000) Binding of the GABA(A) receptor-associated protein (GABARAP) to microtubules and microfilaments suggests involvement of the cytoskeleton in GABARAPGABA(A) receptor interaction. J Neurochem 275:644–655Google Scholar