Abstract
BackgroundVasopressin/oxytocin (VP/OT)-type neuropeptides are well known for their roles as regulators of diuresis, reproductive physiology and social behaviour. However, our knowledge of their functions is largely based on findings from studies on vertebrates and selected protostomian invertebrates. Little is known about the roles of VP/OT-type neuropeptides in deuterostomian invertebrates, which are more closely related to vertebrates than protostomes.ResultsHere, we have identified and functionally characterised a VP/OT-type signalling system comprising the neuropeptide asterotocin and its cognate G-protein coupled receptor in the starfish (sea star) Asterias rubens, a deuterostomian invertebrate belonging to the phylum Echinodermata. Analysis of the distribution of asterotocin and the asterotocin receptor in A. rubens using mRNA in situ hybridisation and immunohistochemistry revealed expression in the central nervous system (radial nerve cords and circumoral nerve ring), the digestive system (including the cardiac stomach) and the body wall and associated appendages. Informed by the anatomy of asterotocin signalling, in vitro pharmacological experiments revealed that asterotocin acts as a muscle relaxant in starfish, contrasting with the myotropic actions of VP/OT-type neuropeptides in vertebrates. Furthermore, in vivo injection of asterotocin had a striking effect on starfish behaviour—triggering fictive feeding where eversion of the cardiac stomach and changes in body posture resemble the unusual extra-oral feeding behaviour of starfish.ConclusionsWe provide a comprehensive characterisation of VP/OT-type signalling in an echinoderm, including a detailed anatomical analysis of the expression of both the VP/OT-type neuropeptide asterotocin and its cognate receptor. Our discovery that asterotocin triggers fictive feeding in starfish provides important new evidence of an evolutionarily ancient role of VP/OT-type neuropeptides as regulators of feeding in animals.
Highlights
Vasopressin/oxytocin (VP/OT)-type neuropeptides are well known for their roles as regulators of diuresis, reproductive physiology and social behaviour
Synthetic asterotocin caused concentration-dependent luminescence in Chinese hamster ovary (CHO) cells transfected with the A. rubens VP/OT-type receptor but had no effect on CHO cells transfected with an empty vector (Fig. 2b)
To obtain new insights into the evolution of VP/OT-type neuropeptide function in the animal kingdom, here we functionally characterised VP/OT-type signalling in an echinoderm—the starfish A. rubens
Summary
Vasopressin/oxytocin (VP/OT)-type neuropeptides are well known for their roles as regulators of diuresis, reproductive physiology and social behaviour. Comparative analysis of genome/ transcriptome sequence data has enabled the discovery of genes encoding VP/OT-type neuropeptides and their putative cognate receptors in many bilaterian animal phyla. This has enabled comparative analysis of the physiological roles of VP/OT-type neuropeptides in species belonging to different phyla [10,11,12]. This has provided evidence that the structures and the functions of VP/OT-type neuropeptides are evolutionarily conserved. Application of reverse genetic techniques in the nematode Caenorhabditis elegans revealed that VP/OT-type signalling is required for normal mating behaviour in this species [16], consistent with the actions of VP and OT in regulating mating behaviour and reproductive physiology in mammals [5]
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