Discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostome
Discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostome
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.
Yañez-Guerra, Luis Alfonso
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Delroisse, Jérôme
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Barreiro-Iglesias, Antón
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Slade, Susan E.
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Scrivens, James H.
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Elphick, Maurice R.
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1 December 2018
Yañez-Guerra, Luis Alfonso
cbca947b-bbf0-4b91-96b0-4a126e3b94b6
Delroisse, Jérôme
901a38d2-3f58-4393-9228-96716cfab9f8
Barreiro-Iglesias, Antón
f0aec648-e32f-4d53-82fd-4cd2de087525
Slade, Susan E.
8b0997e3-514a-4d82-87a1-7c3066e3a500
Scrivens, James H.
12019574-e300-490b-8a96-50fa927bfd89
Elphick, Maurice R.
b4c8b4f9-bb5c-4a0a-bc9d-e941857d4800
Yañez-Guerra, Luis Alfonso, Delroisse, Jérôme, Barreiro-Iglesias, Antón, Slade, Susan E., Scrivens, James H. and Elphick, Maurice R.
(2018)
Discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostome.
Scientific Reports, 8 (1), [7220].
(doi:10.1038/s41598-018-25606-2).
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.
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Published date: 1 December 2018
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Funding Information:
The results presented in this paper have not been published previously in whole or in part. The work reported in this paper was supported by grants from the BBSRC awarded to M.R.E (BB/M001644/1) and J.H.S. (BB/ M001032/1). L.A.Y.G is supported by a PhD studentship awarded by the Mexican Council of Science and Technology (CONACyT studentship no. 418612) and Queen Mary University of London. We are grateful to Philipp Bauknecht and Gáspár Jékely (Max Planck Institute for Developmental Biology, Tübingen, Germany) for providing the Gα16 plasmid and the CHO-G5A cells, which were originally generated by Baubet et al. (Proc Natl Acad Sci USA 97:7260–7265). We are also grateful to Phil Edwards for his help with collecting starfish, Paul Fletcher for maintaining our seawater aquarium and Maria Eugenia Guerra for creating the silhouettes of animals used in Figure 7.
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© 2018 The Author(s).
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Local EPrints ID: 483503
URI: http://eprints.soton.ac.uk/id/eprint/483503
ISSN: 2045-2322
PURE UUID: 33fea99b-7997-4caa-a2b1-9fc8a2f35adb
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Date deposited: 31 Oct 2023 18:24
Last modified: 18 Mar 2024 04:15
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Author:
Luis Alfonso Yañez-Guerra
Author:
Jérôme Delroisse
Author:
Antón Barreiro-Iglesias
Author:
Susan E. Slade
Author:
James H. Scrivens
Author:
Maurice R. Elphick
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