Discovery and functional characterization of neuropeptides in crinoid echinoderms
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...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-12-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2022.1006594/full |
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| author | Alessandra Aleotti Alessandra Aleotti Iain C. Wilkie Luis A. Yañez-Guerra Giacomo Gattoni Giacomo Gattoni Tahshin A. Rahman Richard F. Wademan Zakaryya Ahmad Deyana A. Ivanova Dean C. Semmens Jérôme Delroisse Weigang Cai Esther Odekunle Michaela Egertová Cinzia Ferrario Michela Sugni Francesco Bonasoro Maurice R. Elphick |
| author_facet | Alessandra Aleotti Alessandra Aleotti Iain C. Wilkie Luis A. Yañez-Guerra Giacomo Gattoni Giacomo Gattoni Tahshin A. Rahman Richard F. Wademan Zakaryya Ahmad Deyana A. Ivanova Dean C. Semmens Jérôme Delroisse Weigang Cai Esther Odekunle Michaela Egertová Cinzia Ferrario Michela Sugni Francesco Bonasoro Maurice R. Elphick |
| author_sort | Alessandra Aleotti |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-13T05:03:30Z |
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| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-04-13T05:03:30Z |
| publishDate | 2022-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj.art-61e7d35523414628822c7f9584f523ce2022-12-22T03:01:15ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2022-12-011610.3389/fnins.2022.10065941006594Discovery and functional characterization of neuropeptides in crinoid echinodermsAlessandra Aleotti0Alessandra Aleotti1Iain C. Wilkie2Luis A. Yañez-Guerra3Giacomo Gattoni4Giacomo Gattoni5Tahshin A. Rahman6Richard F. Wademan7Zakaryya Ahmad8Deyana A. Ivanova9Dean C. Semmens10Jérôme Delroisse11Weigang Cai12Esther Odekunle13Michaela Egertová14Cinzia Ferrario15Michela Sugni16Francesco Bonasoro17Maurice R. Elphick18Department of Environmental Science and Policy, University of Milan, Milan, ItalySchool of Biological & Behavioural Sciences, Queen Mary University of London, London, United KingdomInstitute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, United KingdomSchool of Biological & Behavioural Sciences, Queen Mary University of London, London, United KingdomDepartment of Environmental Science and Policy, University of Milan, Milan, ItalySchool of Biological & Behavioural Sciences, Queen Mary University of London, London, United KingdomSchool of Biological & Behavioural Sciences, Queen Mary University of London, London, United KingdomSchool of Biological & Behavioural Sciences, Queen Mary University of London, London, United KingdomSchool of Biological & Behavioural Sciences, Queen Mary University of London, London, United KingdomSchool of Biological & Behavioural Sciences, Queen Mary University of London, London, United KingdomSchool of Biological & Behavioural Sciences, Queen Mary University of London, London, United KingdomSchool of Biological & Behavioural Sciences, Queen Mary University of London, London, United KingdomSchool of Biological & Behavioural Sciences, Queen Mary University of London, London, United KingdomSchool of Biological & Behavioural Sciences, Queen Mary University of London, London, United KingdomSchool of Biological & Behavioural Sciences, Queen Mary University of London, London, United KingdomDepartment of Environmental Science and Policy, University of Milan, Milan, ItalyDepartment of Environmental Science and Policy, University of Milan, Milan, ItalyDepartment of Environmental Science and Policy, University of Milan, Milan, ItalySchool of Biological & Behavioural Sciences, Queen Mary University of London, London, United KingdomNeuropeptides 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.https://www.frontiersin.org/articles/10.3389/fnins.2022.1006594/fullneuropeptidecrinoidechinodermSALMFamidecalcitoninvasopressin/oxytocin |
| spellingShingle | Alessandra Aleotti Alessandra Aleotti Iain C. Wilkie Luis A. Yañez-Guerra Giacomo Gattoni Giacomo Gattoni Tahshin A. Rahman Richard F. Wademan Zakaryya Ahmad Deyana A. Ivanova Dean C. Semmens Jérôme Delroisse Weigang Cai Esther Odekunle Michaela Egertová Cinzia Ferrario Michela Sugni Francesco Bonasoro Maurice R. Elphick Discovery and functional characterization of neuropeptides in crinoid echinoderms Frontiers in Neuroscience neuropeptide crinoid echinoderm SALMFamide calcitonin vasopressin/oxytocin |
| title | Discovery and functional characterization of neuropeptides in crinoid echinoderms |
| title_full | Discovery and functional characterization of neuropeptides in crinoid echinoderms |
| title_fullStr | Discovery and functional characterization of neuropeptides in crinoid echinoderms |
| title_full_unstemmed | Discovery and functional characterization of neuropeptides in crinoid echinoderms |
| title_short | Discovery and functional characterization of neuropeptides in crinoid echinoderms |
| title_sort | discovery and functional characterization of neuropeptides in crinoid echinoderms |
| topic | neuropeptide crinoid echinoderm SALMFamide calcitonin vasopressin/oxytocin |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2022.1006594/full |
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