Receptor deorphanization in an echinoderm reveals kisspeptin evolution and relationship with SALMFamide neuropeptides
Abstract Background Kisspeptins are neuropeptides that regulate reproductive maturation in mammals via G-protein-coupled receptor-mediated stimulation of gonadotropin-releasing hormone secretion from the hypothalamus. Phylogenetic analysis of kisspeptin-type receptors indicates that this neuropeptid...
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| Format: | Article |
| Language: | English |
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BMC
2022-08-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-022-01387-z |
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| author | Nayeli Escudero Castelán Dean C. Semmens Luis Alfonso Yañez Guerra Meet Zandawala Mario dos Reis Susan E. Slade James H. Scrivens Cleidiane G. Zampronio Alexandra M. Jones Olivier Mirabeau Maurice R. Elphick |
| author_facet | Nayeli Escudero Castelán Dean C. Semmens Luis Alfonso Yañez Guerra Meet Zandawala Mario dos Reis Susan E. Slade James H. Scrivens Cleidiane G. Zampronio Alexandra M. Jones Olivier Mirabeau Maurice R. Elphick |
| author_sort | Nayeli Escudero Castelán |
| collection | DOAJ |
| description | Abstract Background Kisspeptins are neuropeptides that regulate reproductive maturation in mammals via G-protein-coupled receptor-mediated stimulation of gonadotropin-releasing hormone secretion from the hypothalamus. Phylogenetic analysis of kisspeptin-type receptors indicates that this neuropeptide signaling system originated in a common ancestor of the Bilateria, but little is known about kisspeptin signaling in invertebrates. Results Contrasting with the occurrence of a single kisspeptin receptor in mammalian species, here, we report the discovery of an expanded family of eleven kisspeptin-type receptors in a deuterostome invertebrate — the starfish Asterias rubens (phylum Echinodermata). Furthermore, neuropeptides derived from four precursor proteins were identified as ligands for six of these receptors. One or more kisspeptin-like neuropeptides derived from two precursor proteins (ArKPP1, ArKPP2) act as ligands for four A. rubens kisspeptin-type receptors (ArKPR1,3,8,9). Furthermore, a family of neuropeptides that act as muscle relaxants in echinoderms (SALMFamides) are ligands for two A. rubens kisspeptin-type receptors (ArKPR6,7). The SALMFamide neuropeptide S1 (or ArS1.4) and a ‘cocktail’ of the seven neuropeptides derived from the S1 precursor protein (ArS1.1-ArS1.7) act as ligands for ArKPR7. The SALMFamide neuropeptide S2 (or ArS2.3) and a ‘cocktail’ of the eight neuropeptides derived from the S2 precursor protein (ArS2.1-ArS2.8) act as ligands for ArKPR6. Conclusions Our findings reveal a remarkable diversity of neuropeptides that act as ligands for kisspeptin-type receptors in starfish and provide important new insights into the evolution of kisspeptin signaling. Furthermore, the discovery of the hitherto unknown relationship of kisspeptins with SALMFamides, neuropeptides that were discovered in starfish prior to the identification of kisspeptins in mammals, presents a radical change in perspective for research on kisspeptin signaling. |
| first_indexed | 2024-04-14T02:57:46Z |
| format | Article |
| id | doaj.art-3c2b8ea9e56e4f6c9bd7b70aaa2e032b |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-14T02:57:46Z |
| publishDate | 2022-08-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-3c2b8ea9e56e4f6c9bd7b70aaa2e032b2022-12-22T02:16:01ZengBMCBMC Biology1741-70072022-08-0120112210.1186/s12915-022-01387-zReceptor deorphanization in an echinoderm reveals kisspeptin evolution and relationship with SALMFamide neuropeptidesNayeli Escudero Castelán0Dean C. Semmens1Luis Alfonso Yañez Guerra2Meet Zandawala3Mario dos Reis4Susan E. Slade5James H. Scrivens6Cleidiane G. Zampronio7Alexandra M. Jones8Olivier Mirabeau9Maurice R. Elphick10Queen Mary University of London, School of Biological & Behavioural SciencesQueen Mary University of London, School of Biological & Behavioural SciencesQueen Mary University of London, School of Biological & Behavioural SciencesQueen Mary University of London, School of Biological & Behavioural SciencesQueen Mary University of London, School of Biological & Behavioural SciencesSchool of Life Sciences, University of WarwickSchool of Life Sciences, University of WarwickSchool of Life Sciences, University of WarwickSchool of Life Sciences, University of WarwickInstitut Pasteur, Université Paris Cité, Bioinformatics and Biostatistics HubQueen Mary University of London, School of Biological & Behavioural SciencesAbstract Background Kisspeptins are neuropeptides that regulate reproductive maturation in mammals via G-protein-coupled receptor-mediated stimulation of gonadotropin-releasing hormone secretion from the hypothalamus. Phylogenetic analysis of kisspeptin-type receptors indicates that this neuropeptide signaling system originated in a common ancestor of the Bilateria, but little is known about kisspeptin signaling in invertebrates. Results Contrasting with the occurrence of a single kisspeptin receptor in mammalian species, here, we report the discovery of an expanded family of eleven kisspeptin-type receptors in a deuterostome invertebrate — the starfish Asterias rubens (phylum Echinodermata). Furthermore, neuropeptides derived from four precursor proteins were identified as ligands for six of these receptors. One or more kisspeptin-like neuropeptides derived from two precursor proteins (ArKPP1, ArKPP2) act as ligands for four A. rubens kisspeptin-type receptors (ArKPR1,3,8,9). Furthermore, a family of neuropeptides that act as muscle relaxants in echinoderms (SALMFamides) are ligands for two A. rubens kisspeptin-type receptors (ArKPR6,7). The SALMFamide neuropeptide S1 (or ArS1.4) and a ‘cocktail’ of the seven neuropeptides derived from the S1 precursor protein (ArS1.1-ArS1.7) act as ligands for ArKPR7. The SALMFamide neuropeptide S2 (or ArS2.3) and a ‘cocktail’ of the eight neuropeptides derived from the S2 precursor protein (ArS2.1-ArS2.8) act as ligands for ArKPR6. Conclusions Our findings reveal a remarkable diversity of neuropeptides that act as ligands for kisspeptin-type receptors in starfish and provide important new insights into the evolution of kisspeptin signaling. Furthermore, the discovery of the hitherto unknown relationship of kisspeptins with SALMFamides, neuropeptides that were discovered in starfish prior to the identification of kisspeptins in mammals, presents a radical change in perspective for research on kisspeptin signaling.https://doi.org/10.1186/s12915-022-01387-zNeuropeptideEvolutionKisspeptinSALMFamideStarfish |
| spellingShingle | Nayeli Escudero Castelán Dean C. Semmens Luis Alfonso Yañez Guerra Meet Zandawala Mario dos Reis Susan E. Slade James H. Scrivens Cleidiane G. Zampronio Alexandra M. Jones Olivier Mirabeau Maurice R. Elphick Receptor deorphanization in an echinoderm reveals kisspeptin evolution and relationship with SALMFamide neuropeptides BMC Biology Neuropeptide Evolution Kisspeptin SALMFamide Starfish |
| title | Receptor deorphanization in an echinoderm reveals kisspeptin evolution and relationship with SALMFamide neuropeptides |
| title_full | Receptor deorphanization in an echinoderm reveals kisspeptin evolution and relationship with SALMFamide neuropeptides |
| title_fullStr | Receptor deorphanization in an echinoderm reveals kisspeptin evolution and relationship with SALMFamide neuropeptides |
| title_full_unstemmed | Receptor deorphanization in an echinoderm reveals kisspeptin evolution and relationship with SALMFamide neuropeptides |
| title_short | Receptor deorphanization in an echinoderm reveals kisspeptin evolution and relationship with SALMFamide neuropeptides |
| title_sort | receptor deorphanization in an echinoderm reveals kisspeptin evolution and relationship with salmfamide neuropeptides |
| topic | Neuropeptide Evolution Kisspeptin SALMFamide Starfish |
| url | https://doi.org/10.1186/s12915-022-01387-z |
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