Initial report of γ-aminobutyric acidergic locomotion regulatory system and its 3-mercaptopropionic acid-sensitivity in metamorphic juvenile of sea urchin, Hemicentrotus pulcherrimus

Abstract

the γ-aminobutyric acid (GABA) signal transmission system (GStS) contributes to larval swimming through the regulation of ciliary beating. However, whether this system also contributes to the primary podia (pp)-generated motility of juveniles remained unclear. the present study aimed to elucidate the involvement of the GSTS in the motility of metamorphic juveniles (juveniles) (1) by immunohistochemically elucidating the location of molecular constituents of the PP, and (2) by inhibiting the activity of GΑΒΑ decarboxylase (GAD) with 3-mercaptopropionic acid (3-MPA). During metamorphosis, the echinus rudiment protrudes its PP out of the body surface in 8-arm plutei. The pp expresses immunopositive signal (-iS) of GAD, GABA, GABA A receptor and tropomyosin, and is constituted with the GABA-iS negative distal tip and the GABA/GAD-iS gaiter region. the latter radiates distal projections to the disc that contains a GAD-iS cellular network. the juvenile body cavity houses a GABA/βiii-tubulin-iS penta-radial ring (prR) that extends branches into each pp and several bridges to the GAD/GABA-iS penta-radial plate (prp) on the oral side but does not reach to the gaiter region. 3-MPA reversibly inhibits the juvenile motility and GABA-IS expression in the PrR/PrP complex. This indicates that the complex is the major contributor to the GABAergic motility in juveniles. The swimming activity of sea urchin plutei is carried out by the body surface ciliary beating and is regulated by various neurotransmitters, including GABA 1 , serotonin 2-4 , and dopamine 5,6. The locomotive activity of juveniles soon after metamorphosis depends on the primary podia (PP) that are derived from the epineural fold of echinus rudiment (EcR) during the late pluteus stages. The PP are accompanied by the radial nerves that extends from the circumoral nerve ring 7,8 and, similar to adult tube feet (TF), it uses a solid substrate to walk by a sucking action that is generated at the disc and the contractile activity of the TF muscle 9. The TF is comprised of water vessels 8 and muscle tissue, which is accompanied by the nervous systems (NS) beneath the ciliated epithelium 10. The NS in the TF is connected to the circumoral nerve ring 8,11 and its movement is regulated by GABA and acetylcholine 12. Thus, GABAergic NS involvement in the motile activity throughout sea urchin development appears to be consistently taken over from the ciliary beating in the larval stage 1,13,14 to creeping movement by the TF of the adult sea urchins. However, how the GABAergic motile organ develops to the adult TF during juvenile development remained unclear. In adult sea urchins, the circumoral synaptotagmin (Syt)-expressing Penta-radial nerve ring appears to control the tube feet movements 15. Thus, the present study aimed to elucidate the following by means of immunohistochemistry of a GABA-immunopositive signal (-IS), glutamate decarboxylase (GAD)-IS, GABA A Receptor (GABA A R)-IS, and tropomyosin (TM)-IS constituents, and through 3-D reconstruction, and pharmaceutical bioa...

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

“…After metamorphosis, the primary podia express GAD, along with GABA(A) receptor, and mobility is severely inhibited under the presence of 3-mercaptopropionic acid [8]. Consistent with the above presence of the GABA signaling cascade in the tube feet of the adult, GABA involvement in tube feet movement in adult sea urchins has been reported as an excitatory neurotransmitter that functions through excitation of cholinergic motoneurons.…”

“…By the 8aPL stage, all eight larval arms were divided into the circumoral ectoderm and the aboral ectoderm regions by CBAS ( Figure 1 J). During this developmental stage, a process for metamorphosis starts that causes dissolution of the larval CBAS [ 8 ]. Two isolated CBASs that are associated with the antero-dorsal epaulets ( Figure 1 J ad-e), and one associated with the posterior epaulet at the most posterior region ( Figure 1 J, po-e), were derived from the circumoral CBAS between the 6aPL and 8aPL stage [ 16 ].…”

“…Thus, the GABAergic signal transmission system (GSTS) consistently plays a major role in sea urchin mobile behavior from the ciliary band, in plutei to primary podia after metamorphosis [8]. However, motility of sea urchin larvae is not solely regulated by the GSTS, but also by the serotonergic system or synaptotagmin (Synt)-expressing neural system [11].…”

Extracellular Vesicle Signatures and Post-Translational Protein Deimination in Purple Sea Urchin (Strongylocentrotus purpuratus) Coelomic Fluid—Novel Insights into Echinodermata Biology

“…It was found to have two predicted disordered regions, whereof the longest was 49aa, and moreover 20 arginines are present in the 452 aa protein. Tubulin plays roles in cytoskeletal rearrangement and has been studied in sea urchins, for example, in relation to cytoskeletal organisation in immune recognition [78], as well as in development and meta-morphosis [113], where post-translational modifications such as acetylation, detyrosination, and polyglutamylation have been studied and found to contribute to the diversification of tubulin functions [114,115]. Sea urchins are furthermore a good model to study antiproliferative drugs, including effects on tubulin dynamics [116].…”

Sea cucumbers: an emerging system in evo-devo

“…The doliolaria nervous system also contains dopaminergic and GABAergic neurons associated with sensory structures including ciliated cells [ 112 ]. These neurotransmitters are involved in the regulation of ciliary beating and swimming behavior in echinoderms and other marine invertebrates [ 39 , 80 , 96 ], therefore an open question is whether the crosstalk of serotonergic, dopaminergic and GABAergic systems regulates these behaviors in holothurians. Moreover, the presence of GABA and dopamine in sensory organs at the pentactula stage suggests that the settlement and subsequent metamorphosis of the larvae is under the control of dopaminergic and GABAergic systems, another feature potentially shared between marine larvae [ 39 ].…”