Discovery and functional characterization of neuropeptides in crinoid echinoderms

Aleotti, A. et al. (2022) Discovery and functional characterization of neuropeptides in crinoid echinoderms. Frontiers in Neuroscience, 16, 1006594. (doi: 10.3389/fnins.2022.1006594) (PMID:36583101) (PMCID:PMC9793003)

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Abstract

Neuropeptides are one of the largest and most diverse families of signaling molecules in animals and, accordingly, they regulate many physiological processes and behaviors. Genome and transcriptome sequencing has enabled the identification of genes encoding neuropeptide precursor proteins in species from a growing variety of taxa, including bilaterian and non-bilaterian animals. Of particular interest are deuterostome invertebrates such as the phylum Echinodermata, which occupies a phylogenetic position that has facilitated reconstruction of the evolution of neuropeptide signaling systems in Bilateria. However, our knowledge of neuropeptide signaling in echinoderms is largely based on bioinformatic and experimental analysis of eleutherozoans—Asterozoa (starfish and brittle stars) and Echinozoa (sea urchins and sea cucumbers). Little is known about neuropeptide signaling in crinoids (feather stars and sea lilies), which are a sister clade to the Eleutherozoa. Therefore, we have analyzed transcriptome/genome sequence data from three feather star species, Anneissia japonica, Antedon mediterranea, and Florometra serratissima, to produce the first comprehensive identification of neuropeptide precursors in crinoids. These include representatives of bilaterian neuropeptide precursor families and several predicted crinoid neuropeptide precursors. Using A. mediterranea as an experimental model, we have investigated the expression of selected neuropeptides in larvae (doliolaria), post-metamorphic pentacrinoids and adults, providing new insights into the cellular architecture of crinoid nervous systems. Thus, using mRNA in situ hybridization F-type SALMFamide precursor transcripts were revealed in a previously undescribed population of peptidergic cells located dorso-laterally in doliolaria. Furthermore, using immunohistochemistry a calcitonin-type neuropeptide was revealed in the aboral nerve center, circumoral nerve ring and oral tube feet in pentacrinoids and in the ectoneural and entoneural compartments of the nervous system in adults. Moreover, functional analysis of a vasopressin/oxytocin-type neuropeptide (crinotocin), which is expressed in the brachial nerve of the arms in A. mediterranea, revealed that this peptide causes a dose-dependent change in the mechanical behavior of arm preparations in vitro—the first reported biological action of a neuropeptide in a crinoid. In conclusion, our findings provide new perspectives on neuropeptide signaling in echinoderms and the foundations for further exploration of neuropeptide expression/function in crinoids as a sister clade to eleutherozoan echinoderms.

Item Type:Articles
Additional Information:Funding: This research was supported by a Leverhulme Trust Emeritus Fellowship (EM-2016-018) awarded to IW, a BBSRC grant (BB/M001644/1) awarded to MRE, and Erasmus Scholarships awarded to AA (Erasmus+ 2015/16 and Erasmus+ 2016/17).
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Wilkie, Dr Iain
Authors: Aleotti, A., Wilkie, I. C., Yañez-Guerra, L. A., Gattoni, G., Rahman, T. A., Wademan, R. F., Ahmad, Z., Ivanova, D. A., Semmens, D. C., Delroisse, J., Cai, W., Odekunle, E., Egertová, M., Ferrario, C., Sugni, M., Bonasoro, F., and Elphick, M. R.
College/School:College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine
Journal Name:Frontiers in Neuroscience
Publisher:Frontiers Media
ISSN:1662-4548
ISSN (Online):1662-453X
Copyright Holders:Copyright © 2022 Aleotti, Wilkie, Yañez-Guerra, Gattoni, Rahman, Wademan, Ahmad, Ivanova, Semmens, Delroisse, Cai, Odekunle, Egertová, Ferrario, Sugni, Bonasoro and Elphick
First Published:First published in Frontiers in Neuroscience 16: 1006594
Publisher Policy:Reproduced under a Creative Commons License

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