Discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostome

Abstract Neuropeptides are diverse and evolutionarily ancient regulators of physiological/behavioural processes in animals. Here we have investigated the evolution and comparative physiology of luqin-type neuropeptide signalling, which has been characterised previously in protostomian invertebrates....

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Main Authors: Luis Alfonso Yañez-Guerra, Jérôme Delroisse, Antón Barreiro-Iglesias, Susan E. Slade, James H. Scrivens, Maurice R. Elphick
Format: Article
Language:English
Published: Nature Publishing Group 2018-05-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-018-25606-2
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spelling doaj-6ff3d2f780ce4554bdc67b77a6e7fbc22020-12-08T06:22:56ZengNature Publishing GroupScientific Reports2045-23222018-05-018111410.1038/s41598-018-25606-2Discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostomeLuis Alfonso Yañez-Guerra0Jérôme Delroisse1Antón Barreiro-Iglesias2Susan E. Slade3James H. Scrivens4Maurice R. Elphick5Queen Mary University of London, School of Biological & Chemical SciencesQueen Mary University of London, School of Biological & Chemical SciencesQueen Mary University of London, School of Biological & Chemical SciencesWaters/Warwick Centre for BioMedical Mass Spectrometry and Proteomics, School of Life Sciences, University of WarwickWaters/Warwick Centre for BioMedical Mass Spectrometry and Proteomics, School of Life Sciences, University of WarwickQueen Mary University of London, School of Biological & Chemical SciencesAbstract Neuropeptides are diverse and evolutionarily ancient regulators of physiological/behavioural processes in animals. Here we have investigated the evolution and comparative physiology of luqin-type neuropeptide signalling, which has been characterised previously in protostomian invertebrates. Phylogenetic analysis indicates that luqin-type receptors and tachykinin-type receptors are paralogous and probably originated in a common ancestor of the Bilateria. In the deuterostomian lineage, luqin-type signalling has been lost in chordates but interestingly it has been retained in ambulacrarians. Therefore, here we characterised luqin-type signalling for the first time in an ambulacrarian – the starfish Asterias rubens (phylum Echinodermata). A luqin-like neuropeptide with a C-terminal RWamide motif (ArLQ; EEKTRFPKFMRW-NH2) was identified as the ligand for two luqin-type receptors in A. rubens, ArLQR1 and ArLQR2. Furthermore, analysis of the expression of the ArLQ precursor using mRNA in situ hybridisation revealed expression in the nervous system, digestive system and locomotory organs (tube feet) and in vitro pharmacology revealed that ArLQ causes dose-dependent relaxation of tube feet. Accordingly, previous studies have revealed that luqin-type signalling regulates feeding and locomotor activity in protostomes. In conclusion, our phylogenetic analysis combined with characterisation of luqin-type signalling in a deuterostome has provided new insights into neuropeptide evolution and function in the animal kingdom.https://doi.org/10.1038/s41598-018-25606-2
collection DOAJ
language English
format Article
sources DOAJ
author Luis Alfonso Yañez-Guerra
Jérôme Delroisse
Antón Barreiro-Iglesias
Susan E. Slade
James H. Scrivens
Maurice R. Elphick
spellingShingle Luis Alfonso Yañez-Guerra
Jérôme Delroisse
Antón Barreiro-Iglesias
Susan E. Slade
James H. Scrivens
Maurice R. Elphick
Discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostome
Scientific Reports
author_facet Luis Alfonso Yañez-Guerra
Jérôme Delroisse
Antón Barreiro-Iglesias
Susan E. Slade
James H. Scrivens
Maurice R. Elphick
author_sort Luis Alfonso Yañez-Guerra
title Discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostome
title_short Discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostome
title_full Discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostome
title_fullStr Discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostome
title_full_unstemmed Discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostome
title_sort discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostome
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2018-05-01
description Abstract Neuropeptides are diverse and evolutionarily ancient regulators of physiological/behavioural processes in animals. Here we have investigated the evolution and comparative physiology of luqin-type neuropeptide signalling, which has been characterised previously in protostomian invertebrates. Phylogenetic analysis indicates that luqin-type receptors and tachykinin-type receptors are paralogous and probably originated in a common ancestor of the Bilateria. In the deuterostomian lineage, luqin-type signalling has been lost in chordates but interestingly it has been retained in ambulacrarians. Therefore, here we characterised luqin-type signalling for the first time in an ambulacrarian – the starfish Asterias rubens (phylum Echinodermata). A luqin-like neuropeptide with a C-terminal RWamide motif (ArLQ; EEKTRFPKFMRW-NH2) was identified as the ligand for two luqin-type receptors in A. rubens, ArLQR1 and ArLQR2. Furthermore, analysis of the expression of the ArLQ precursor using mRNA in situ hybridisation revealed expression in the nervous system, digestive system and locomotory organs (tube feet) and in vitro pharmacology revealed that ArLQ causes dose-dependent relaxation of tube feet. Accordingly, previous studies have revealed that luqin-type signalling regulates feeding and locomotor activity in protostomes. In conclusion, our phylogenetic analysis combined with characterisation of luqin-type signalling in a deuterostome has provided new insights into neuropeptide evolution and function in the animal kingdom.
url https://doi.org/10.1038/s41598-018-25606-2
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