Discovery and functional characterisation of novel neuropeptide signalling systems in echinoderms

Abstract

Neuropeptides are evolutionarily ancient mediators of neuronal signalling that regulate a diverse range of physiological processes and behaviours. Recent advances in comparative genomics/transcriptomics are providing opportunities to analyse neuropeptide systems in a wider range of phyla. The echinoderms (e.g. starfish, sea urchins and sea cucumbers) are of particular interest in this respect because as deuterostomian invertebrates they occupy an intermediate position in animal phylogeny, bridging model protostomian invertebrates (e.g. Drosophila) to the vertebrates. Herein, the common European starfish Asterias rubens has been established as a model system for neuropeptide research. Generation and analysis of a neural transcriptome dataset from A. rubens has enabled the identification of thirty-five novel neuropeptide precursors and a number of candidate receptors. Interestingly, precursors of two kisspeptin-type peptides (the first identified in a non-chordate species), a melanin-concentrating hormone-type peptide (the first identified outside of the vertebrates) and two tachykinin-type peptides (the first identified in an ambulacrarian species) were identified. Discovery of this repertoire of neuropeptide precursors has provided the foundation for a comprehensive analysis of the physiological functions of neuropeptides in starfish. Investigation of the physiological roles of two neuropeptides – a vasopressin/oxytocin-type peptide (“asterotocin”) and an NG peptide (“NGFFYamide”) – has revealed roles in the remarkable process of extraoral feeding in starfish. Discovery of neuropeptides that trigger cardiac stomach eversion (asterotocin) and retraction (NGFFYamide) provides a novel insight into the neural regulation of starfish feeding and a rationale for chemically based strategies to control starfish that feed on economically important shellfish or protected marine fauna. Finally, characterisation of the receptor for the NG peptide NGFFFamide in the sea urchin Strongylocentrotus purpuratus has unified a bilaterian neuropeptide family that includes neuropeptide-S-type peptides in tetrapod vertebrates, NG peptides in deuterostomian invertebrates and crustacean cardioactive peptide-type peptides in protostomian invertebrates.