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Receptor deorphanization in an echinoderm reveals kisspeptin evolution and relationship with SALMFamide neuropeptides.

Escudero Castelán, N; Semmens, DC; Guerra, LAY; Zandawala, M; Dos Reis, M; Slade, SE; Scrivens, JH; Zampronio, CG; Jones, AM; Mirabeau, O; et al. Escudero Castelán, N; Semmens, DC; Guerra, LAY; Zandawala, M; Dos Reis, M; Slade, SE; Scrivens, JH; Zampronio, CG; Jones, AM; Mirabeau, O; Elphick, MR (2022) Receptor deorphanization in an echinoderm reveals kisspeptin evolution and relationship with SALMFamide neuropeptides. BMC Biol, 20 (1). p. 187. ISSN 1741-7007 https://doi.org/10.1186/s12915-022-01387-z
SGUL Authors: Semmens, Dean Colin

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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.

Item Type: Article
Additional Information: © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
Keywords: Evolution, Kisspeptin, Neuropeptide, SALMFamide, Starfish, Amino Acid Sequence, Animals, Echinodermata, Kisspeptins, Ligands, Mammals, Neuropeptides, Phylogeny, Starfish, Animals, Mammals, Echinodermata, Starfish, Neuropeptides, Ligands, Phylogeny, Amino Acid Sequence, Kisspeptins, 06 Biological Sciences, Developmental Biology
SGUL Research Institute / Research Centre: Academic Structure > Institute of Medical & Biomedical Education (IMBE)
Academic Structure > Institute of Medical & Biomedical Education (IMBE) > Centre for Biomedical Education (INMEBE)
Journal or Publication Title: BMC Biol
ISSN: 1741-7007
Language: eng
Dates:
DateEvent
24 August 2022Published
9 August 2022Accepted
Publisher License: Creative Commons: Attribution 4.0
Projects:
Project IDFunderFunder ID
RPG-2013-351Leverhulme Trusthttp://dx.doi.org/10.13039/501100000275
RPG-2016-353Leverhulme Trusthttp://dx.doi.org/10.13039/501100000275
BB/M001644/1Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
BB/M001032/1Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
471864CONACyT (Mexican Council of Science and Technology)UNSPECIFIED
418612CONACyT (Mexican Council of Science and Technology)UNSPECIFIED
PubMed ID: 36002813
Go to PubMed abstract
URI: https://openaccess.sgul.ac.uk/id/eprint/114734
Publisher's version: https://doi.org/10.1186/s12915-022-01387-z

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