Abstract
BackgroundThe swimming activity of sea urchin larvae is dependent on the ciliary band (CB) on the larval surface and is regulated by several neurotransmitters, including serotonin (5HT), dopamine, and γ-aminobutyric acid (GABA). However, the CB signal transmission mechanism remains unknown. The present study investigated the structural relationship between the CB and external signal receptors by immunohistochemical and transmission electron microscopic analyses of sea urchin, Hemicentrotus pulcherrimus, larvae.ResultsGlutamate decarboxylase (GAD; GABA synthetase) was detected in a strand of multiple cells along the circumoral CB in 6-arm plutei. The GAD-expressing strand was closely associated with the CB on the oral ectoderm side. The ciliary band-associated strand (CBAS) also expressed the 5HT receptor (5HThpr) and encephalopsin (ECPN) throughout the cytoplasm and comprised 1- to 2-μm diameter axon-like long stretched regions and sporadic 6- to 7-μm diameter bulbous nucleated regions (perikarya) that protruded into the oral ectoderm side. Besides the laterally polarized morphology of the CBAS cells, Epith-2, which is the epithelial lateral cell surface-specific protein of the sea urchin embryo and larva, was expressed exclusively by perikarya but not by the axon-like regions. The CBAS exposed its narrow apical surface on the larval epithelium between the CB and squamous cells and formed adherens junctions (AJs) on the apical side between them. Despite the presence of the CBAS axon-like regions, tubulins, such as α-, β-, and acetylated α-tubulins, were not detected. However, the neuroendocrine cell marker protein synaptophysin was detected in the axon-like regions and in bouton-like protrusions that contained numerous small ultrastructural vesicles.ConclusionsThe unique morphology of the CBAS in the sea urchin larva epithelium had not been reported. The CBAS expresses a remarkable number of receptors to environmental stimuli and proteins that are probably involved in signal transmission to the CB. The properties of the CBAS explain previous reports that larval swimming is triggered by environmental stimuli and suggest crosstalk among receptors and potential plural sensory functions of the CBAS.
Highlights
The swimming activity of sea urchin larvae is dependent on the ciliary band (CB) on the larval surface and is regulated by several neurotransmitters, including serotonin (5HT), dopamine, and γ-aminobutyric acid (GABA)
The major driving force for sea urchin larval swimming is generated by beating of cilia on the ciliary band (CB) of larval arms [15], which is regulated by DA [10, 16], 5HT [8, 9, 16,17,18], and GABA [7]. 5HT initiates the cytoplasmic calcium ion-releasing signal to the ciliated epithelial cells through the coelomic network of 5HT receptor (5HThpr)-expressing cells [8, 9]
Because the CB formed at the border between the oral ectoderm and aboral ectoderm (Fig. 1a, b, d), Hp-dopamine receptor D1 (DRD1) was chosen as a CB molecular marker to specify the exact location of the CBassociated strand (CBAS) to the CB
Summary
The swimming activity of sea urchin larvae is dependent on the ciliary band (CB) on the larval surface and is regulated by several neurotransmitters, including serotonin (5HT), dopamine, and γ-aminobutyric acid (GABA). Sea urchin larvae respond to other neurotransmitters, such as serotonin (5HT; [8, 9]) and dopamine (DA; [10]) in addition to light [11]. The CBassociated strand (CBAS) of GADCs appears at about the 2-arm pluteus stage and encircles the oral ectoderm by the 6-arm pluteus stage [7] These previous reports suggest that the CBAS functions as a GABA sensory organ. ECPN is expressed in a subgroup of blastocoelar cells along with 5HT receptor (5HThpr) [8], despite that these cells are not closely localized with the CB [11]
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