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Echinoderms provide missing link in the evolution of PrRP/sNPF-type neuropeptide signalling

Echinoderms provide missing link in the evolution of PrRP/sNPF-type neuropeptide signalling
Echinoderms provide missing link in the evolution of PrRP/sNPF-type neuropeptide signalling

Neuropeptide signalling systems comprising peptide ligands and cognate receptors are evolutionarily ancient regulators of physiology and behaviour. However, there are challenges associated with determination of orthology between neuropeptides in different taxa. Orthologs of vertebrate neuropeptide-Y (NPY) known as neuropeptide-F (NPF) have been identified in protostome invertebrates, whilst prolactin-releasing peptide (PrRP) and short neuropeptide-F (sNPF) have been identified as paralogs of NPY/NPF in vertebrates and protostomes, respectively. Here we investigated the occurrence of NPY/NPF/PrRP/sNPF-related signalling systems in a deuterostome invertebrate phylum – the Echinodermata. Analysis of transcriptome/genome sequence data revealed loss of NPY/NPF-type signalling, but orthologs of PrRP-type neuropeptides and sNPF/PrRP-type receptors were identified in echinoderms. Furthermore, experimental studies revealed that the PrRP-type neuropeptide pQDRSKAMQAERTGQLRRLNPRF-NH2 is a potent ligand for a sNPF/PrRP-type receptor in the starfish Asterias rubens. Our findings indicate that PrRP-type and sNPF-type signalling systems are orthologous and originated as a paralog of NPY/NPF-type signalling in Urbilateria.

2050-084X
1-23
Yañez-Guerra, Luis Alfonso
cbca947b-bbf0-4b91-96b0-4a126e3b94b6
Zhong, Xingxing
a599b69c-e186-4b5e-b662-1c3e107a6c06
Moghul, Ismail
603853aa-f288-4981-b21f-fb82c949db30
Butts, Thomas
f30ebab1-2624-41de-b32d-2461fe771c16
Zampronio, Cleidiane G.
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Jones, Alexandra M.
81a5d813-12ce-4298-bb1a-d206c2f8c907
Mirabeau, Olivier
928933a2-7435-4052-81cb-2e482c5073cb
Elphick, Maurice R.
b4c8b4f9-bb5c-4a0a-bc9d-e941857d4800
Yañez-Guerra, Luis Alfonso
cbca947b-bbf0-4b91-96b0-4a126e3b94b6
Zhong, Xingxing
a599b69c-e186-4b5e-b662-1c3e107a6c06
Moghul, Ismail
603853aa-f288-4981-b21f-fb82c949db30
Butts, Thomas
f30ebab1-2624-41de-b32d-2461fe771c16
Zampronio, Cleidiane G.
3fd9b7c1-87d2-485a-86bf-7b8f66d53de4
Jones, Alexandra M.
81a5d813-12ce-4298-bb1a-d206c2f8c907
Mirabeau, Olivier
928933a2-7435-4052-81cb-2e482c5073cb
Elphick, Maurice R.
b4c8b4f9-bb5c-4a0a-bc9d-e941857d4800

Yañez-Guerra, Luis Alfonso, Zhong, Xingxing, Moghul, Ismail, Butts, Thomas, Zampronio, Cleidiane G., Jones, Alexandra M., Mirabeau, Olivier and Elphick, Maurice R. (2020) Echinoderms provide missing link in the evolution of PrRP/sNPF-type neuropeptide signalling. eLife, 9, 1-23, [e57640]. (doi:10.7554/eLife.57640).

Record type: Article

Abstract

Neuropeptide signalling systems comprising peptide ligands and cognate receptors are evolutionarily ancient regulators of physiology and behaviour. However, there are challenges associated with determination of orthology between neuropeptides in different taxa. Orthologs of vertebrate neuropeptide-Y (NPY) known as neuropeptide-F (NPF) have been identified in protostome invertebrates, whilst prolactin-releasing peptide (PrRP) and short neuropeptide-F (sNPF) have been identified as paralogs of NPY/NPF in vertebrates and protostomes, respectively. Here we investigated the occurrence of NPY/NPF/PrRP/sNPF-related signalling systems in a deuterostome invertebrate phylum – the Echinodermata. Analysis of transcriptome/genome sequence data revealed loss of NPY/NPF-type signalling, but orthologs of PrRP-type neuropeptides and sNPF/PrRP-type receptors were identified in echinoderms. Furthermore, experimental studies revealed that the PrRP-type neuropeptide pQDRSKAMQAERTGQLRRLNPRF-NH2 is a potent ligand for a sNPF/PrRP-type receptor in the starfish Asterias rubens. Our findings indicate that PrRP-type and sNPF-type signalling systems are orthologous and originated as a paralog of NPY/NPF-type signalling in Urbilateria.

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More information

Published date: 1 June 2020
Additional Information: Funding Information: The work reported in this paper was supported by grants from the BBSRC awarded to MRE (BB/ M001644/1) and AMJ (BB/M001032/1). LAYG was supported by a PhD studentship awarded by the Mexican Council of Science and Technology (CONACyT studentship no. 418612) and Queen Mary University of London and by a Leverhulme Trust grant (RPG-2016–353) awarded to MRE. XZ was supported by a PhD studentship awarded by the China Scholarship Council and Queen Mary University of London. We are grateful to Gáspár Jékely (University of Exeter) for providing the CHO-K1 (G5A) cell line used here for receptor deorphanisation assays. Funding Information: Biotechnology and Biological Sciences Research Council BB/M001644/1 Maurice R Elphick Biotechnology and Biological Sciences Research Council BB/M001032/1 Alexandra M Jones CONACyT CONACyT studentship no. 418612 Luis Alfonso Yan˜ ez-Guerra Leverhulme Trust RPG-2016-353 Maurice R Elphick China Scholarship Council Xingxing Zhong. Publisher Copyright: © Yañez-Guerra et al.

Identifiers

Local EPrints ID: 483964
URI: http://eprints.soton.ac.uk/id/eprint/483964
ISSN: 2050-084X
PURE UUID: 6fe40c29-a90e-45ea-8b6f-89cf92041f8b
ORCID for Luis Alfonso Yañez-Guerra: ORCID iD orcid.org/0000-0002-2523-1310

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Date deposited: 07 Nov 2023 18:55
Last modified: 18 Mar 2024 04:15

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Contributors

Author: Luis Alfonso Yañez-Guerra ORCID iD
Author: Xingxing Zhong
Author: Ismail Moghul
Author: Thomas Butts
Author: Cleidiane G. Zampronio
Author: Alexandra M. Jones
Author: Olivier Mirabeau
Author: Maurice R. Elphick

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