Molecular and functional characterization of somatostatin-type signalling in a deuterostome invertebrate
Molecular and functional characterization of somatostatin-type signalling in a deuterostome invertebrate
Somatostatin (SS) and allatostatin-C (ASTC) are structurally and evolutionarily related neuropeptides that act as inhibitory regulators of physiological processes in mammals and insects, respectively. Here, we report the first molecular and functional characterization of SS/ASTC-type signalling in a deuterostome invertebrate - the starfish Asterias rubens (phylum Echinodermata). Two SS/ASTC-type precursors were identified in A. rubens (ArSSP1 and ArSSP2) and the structures of neuropeptides derived from these proteins (ArSS1 and ArSS2) were analysed using mass spectrometry. Pharmacological characterization of three cloned A. rubens SS/ASTC-type receptors (ArSSR1-3) revealed that ArSS2, but not ArSS1, acts as a ligand for all three receptors. Analysis of ArSS2 expression in A. rubens using mRNA in situ hybridization and immunohistochemistry revealed stained cells/fibres in the central nervous system, the digestive system (e.g. cardiac stomach) and the body wall and its appendages (e.g. tube feet). Furthermore, in vitro pharmacological tests revealed that ArSS2 causes dose-dependent relaxation of tube foot and cardiac stomach preparations, while injection of ArSS2 in vivo causes partial eversion of the cardiac stomach. Our findings provide new insights into the molecular evolution of SS/ASTC-type signalling in the animal kingdom and reveal an ancient role of SS-type neuropeptides as inhibitory regulators of muscle contractility.
evolution, muscle, neuropeptide, receptor, somatostatin, starfish
Zhang, Ya
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Yañez Guerra, Luis Alfonso
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Egertová, Michaela
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Zampronio, Cleidiane G.
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Jones, Alexandra M.
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Elphick, Maurice R.
b4c8b4f9-bb5c-4a0a-bc9d-e941857d4800
1 September 2020
Zhang, Ya
1820fb16-8a49-4749-9964-12bcbded2641
Yañez Guerra, Luis Alfonso
cbca947b-bbf0-4b91-96b0-4a126e3b94b6
Egertová, Michaela
9a68b847-d995-40b0-8d94-3918037aed83
Zampronio, Cleidiane G.
3fd9b7c1-87d2-485a-86bf-7b8f66d53de4
Jones, Alexandra M.
81a5d813-12ce-4298-bb1a-d206c2f8c907
Elphick, Maurice R.
b4c8b4f9-bb5c-4a0a-bc9d-e941857d4800
Zhang, Ya, Yañez Guerra, Luis Alfonso, Egertová, Michaela, Zampronio, Cleidiane G., Jones, Alexandra M. and Elphick, Maurice R.
(2020)
Molecular and functional characterization of somatostatin-type signalling in a deuterostome invertebrate.
Open Biology, 10 (9), [200172].
(doi:10.1098/rsob.200172).
Abstract
Somatostatin (SS) and allatostatin-C (ASTC) are structurally and evolutionarily related neuropeptides that act as inhibitory regulators of physiological processes in mammals and insects, respectively. Here, we report the first molecular and functional characterization of SS/ASTC-type signalling in a deuterostome invertebrate - the starfish Asterias rubens (phylum Echinodermata). Two SS/ASTC-type precursors were identified in A. rubens (ArSSP1 and ArSSP2) and the structures of neuropeptides derived from these proteins (ArSS1 and ArSS2) were analysed using mass spectrometry. Pharmacological characterization of three cloned A. rubens SS/ASTC-type receptors (ArSSR1-3) revealed that ArSS2, but not ArSS1, acts as a ligand for all three receptors. Analysis of ArSS2 expression in A. rubens using mRNA in situ hybridization and immunohistochemistry revealed stained cells/fibres in the central nervous system, the digestive system (e.g. cardiac stomach) and the body wall and its appendages (e.g. tube feet). Furthermore, in vitro pharmacological tests revealed that ArSS2 causes dose-dependent relaxation of tube foot and cardiac stomach preparations, while injection of ArSS2 in vivo causes partial eversion of the cardiac stomach. Our findings provide new insights into the molecular evolution of SS/ASTC-type signalling in the animal kingdom and reveal an ancient role of SS-type neuropeptides as inhibitory regulators of muscle contractility.
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Accepted/In Press date: 6 August 2020
Published date: 1 September 2020
Additional Information:
Funding Information:
The work reported in this paper was supported by grants from the BBSRC awarded to M.R.E (grant no. BB/M001644/1) and A.M.J. (grant no. BB/M001032/1). Y.Z. was supported by a PhD studentship awarded by the China Scholarship Council and Queen Mary University of London. L.A.Y.G 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 (grant no. RPG-2016-353) awarded to M.R.E.
Publisher Copyright:
© 2020 The Authors.
Keywords:
evolution, muscle, neuropeptide, receptor, somatostatin, starfish
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Local EPrints ID: 483966
URI: http://eprints.soton.ac.uk/id/eprint/483966
PURE UUID: 9640ee6f-e386-438f-8271-5a4b6ac05f59
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Date deposited: 07 Nov 2023 18:55
Last modified: 18 Mar 2024 04:15
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Contributors
Author:
Ya Zhang
Author:
Luis Alfonso Yañez Guerra
Author:
Michaela Egertová
Author:
Cleidiane G. Zampronio
Author:
Alexandra M. Jones
Author:
Maurice R. Elphick
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