Ancient role of sulfakinin/cholecystokinin-type signalling in inhibitory regulation of feeding processes revealed in an echinoderm

Sulfakinin (SK)/cholecystokinin (CCK)-type neuropeptides regulate feeding and digestion in protostomes (e.g. insects) and chordates. Here, we characterised SK/CCK-type signalling for the first time in a non-chordate deuterostome – the starfish Asterias rubens (phylum Echinodermata). In this species,...

Full description

Bibliographic Details
Main Authors: Ana B Tinoco, Antón Barreiro-Iglesias, Luis Alfonso Yañez Guerra, Jérôme Delroisse, Ya Zhang, Elizabeth F Gunner, Cleidiane G Zampronio, Alexandra M Jones, Michaela Egertová, Maurice R Elphick
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-09-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/65667
id doaj-dc7723c7cb414f809705a7edef0e5a3b
record_format Article
spelling doaj-dc7723c7cb414f809705a7edef0e5a3b2021-09-09T07:15:13ZengeLife Sciences Publications LtdeLife2050-084X2021-09-011010.7554/eLife.65667Ancient role of sulfakinin/cholecystokinin-type signalling in inhibitory regulation of feeding processes revealed in an echinodermAna B Tinoco0https://orcid.org/0000-0003-0525-4475Antón Barreiro-Iglesias1https://orcid.org/0000-0002-7507-080XLuis Alfonso Yañez Guerra2https://orcid.org/0000-0002-2523-1310Jérôme Delroisse3https://orcid.org/0000-0002-9233-6470Ya Zhang4https://orcid.org/0000-0002-2158-0660Elizabeth F Gunner5Cleidiane G Zampronio6https://orcid.org/0000-0003-0934-0792Alexandra M Jones7https://orcid.org/0000-0003-2571-8708Michaela Egertová8Maurice R Elphick9https://orcid.org/0000-0002-9169-0048Queen Mary University of London, School of Biological & Behavioural Sciences, London, United KingdomQueen Mary University of London, School of Biological & Behavioural Sciences, London, United KingdomQueen Mary University of London, School of Biological & Behavioural Sciences, London, United KingdomQueen Mary University of London, School of Biological & Behavioural Sciences, London, United KingdomQueen Mary University of London, School of Biological & Behavioural Sciences, London, United KingdomQueen Mary University of London, School of Biological & Behavioural Sciences, London, United KingdomSchool of Life Sciences and Proteomics, Research Technology Platform, University of Warwick, Coventry, United KingdomSchool of Life Sciences and Proteomics, Research Technology Platform, University of Warwick, Coventry, United KingdomQueen Mary University of London, School of Biological & Behavioural Sciences, London, United KingdomQueen Mary University of London, School of Biological & Behavioural Sciences, London, United KingdomSulfakinin (SK)/cholecystokinin (CCK)-type neuropeptides regulate feeding and digestion in protostomes (e.g. insects) and chordates. Here, we characterised SK/CCK-type signalling for the first time in a non-chordate deuterostome – the starfish Asterias rubens (phylum Echinodermata). In this species, two neuropeptides (ArSK/CCK1, ArSK/CCK2) derived from the precursor protein ArSK/CCKP act as ligands for an SK/CCK-type receptor (ArSK/CCKR) and these peptides/proteins are expressed in the nervous system, digestive system, tube feet, and body wall. Furthermore, ArSK/CCK1 and ArSK/CCK2 cause dose-dependent contraction of cardiac stomach, tube foot, and apical muscle preparations in vitro, and injection of these neuropeptides in vivo triggers cardiac stomach retraction and inhibition of the onset of feeding in A. rubens. Thus, an evolutionarily ancient role of SK/CCK-type neuropeptides as inhibitory regulators of feeding-related processes in the Bilateria has been conserved in the unusual and unique context of the extra-oral feeding behaviour and pentaradial body plan of an echinoderm.https://elifesciences.org/articles/65667Asterias rubensstarfishsulfakinin/cholecystokininneuropeptidesfeedingreceptors
collection DOAJ
language English
format Article
sources DOAJ
author Ana B Tinoco
Antón Barreiro-Iglesias
Luis Alfonso Yañez Guerra
Jérôme Delroisse
Ya Zhang
Elizabeth F Gunner
Cleidiane G Zampronio
Alexandra M Jones
Michaela Egertová
Maurice R Elphick
spellingShingle Ana B Tinoco
Antón Barreiro-Iglesias
Luis Alfonso Yañez Guerra
Jérôme Delroisse
Ya Zhang
Elizabeth F Gunner
Cleidiane G Zampronio
Alexandra M Jones
Michaela Egertová
Maurice R Elphick
Ancient role of sulfakinin/cholecystokinin-type signalling in inhibitory regulation of feeding processes revealed in an echinoderm
eLife
Asterias rubens
starfish
sulfakinin/cholecystokinin
neuropeptides
feeding
receptors
author_facet Ana B Tinoco
Antón Barreiro-Iglesias
Luis Alfonso Yañez Guerra
Jérôme Delroisse
Ya Zhang
Elizabeth F Gunner
Cleidiane G Zampronio
Alexandra M Jones
Michaela Egertová
Maurice R Elphick
author_sort Ana B Tinoco
title Ancient role of sulfakinin/cholecystokinin-type signalling in inhibitory regulation of feeding processes revealed in an echinoderm
title_short Ancient role of sulfakinin/cholecystokinin-type signalling in inhibitory regulation of feeding processes revealed in an echinoderm
title_full Ancient role of sulfakinin/cholecystokinin-type signalling in inhibitory regulation of feeding processes revealed in an echinoderm
title_fullStr Ancient role of sulfakinin/cholecystokinin-type signalling in inhibitory regulation of feeding processes revealed in an echinoderm
title_full_unstemmed Ancient role of sulfakinin/cholecystokinin-type signalling in inhibitory regulation of feeding processes revealed in an echinoderm
title_sort ancient role of sulfakinin/cholecystokinin-type signalling in inhibitory regulation of feeding processes revealed in an echinoderm
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-09-01
description Sulfakinin (SK)/cholecystokinin (CCK)-type neuropeptides regulate feeding and digestion in protostomes (e.g. insects) and chordates. Here, we characterised SK/CCK-type signalling for the first time in a non-chordate deuterostome – the starfish Asterias rubens (phylum Echinodermata). In this species, two neuropeptides (ArSK/CCK1, ArSK/CCK2) derived from the precursor protein ArSK/CCKP act as ligands for an SK/CCK-type receptor (ArSK/CCKR) and these peptides/proteins are expressed in the nervous system, digestive system, tube feet, and body wall. Furthermore, ArSK/CCK1 and ArSK/CCK2 cause dose-dependent contraction of cardiac stomach, tube foot, and apical muscle preparations in vitro, and injection of these neuropeptides in vivo triggers cardiac stomach retraction and inhibition of the onset of feeding in A. rubens. Thus, an evolutionarily ancient role of SK/CCK-type neuropeptides as inhibitory regulators of feeding-related processes in the Bilateria has been conserved in the unusual and unique context of the extra-oral feeding behaviour and pentaradial body plan of an echinoderm.
topic Asterias rubens
starfish
sulfakinin/cholecystokinin
neuropeptides
feeding
receptors
url https://elifesciences.org/articles/65667
work_keys_str_mv AT anabtinoco ancientroleofsulfakinincholecystokinintypesignallingininhibitoryregulationoffeedingprocessesrevealedinanechinoderm
AT antonbarreiroiglesias ancientroleofsulfakinincholecystokinintypesignallingininhibitoryregulationoffeedingprocessesrevealedinanechinoderm
AT luisalfonsoyanezguerra ancientroleofsulfakinincholecystokinintypesignallingininhibitoryregulationoffeedingprocessesrevealedinanechinoderm
AT jeromedelroisse ancientroleofsulfakinincholecystokinintypesignallingininhibitoryregulationoffeedingprocessesrevealedinanechinoderm
AT yazhang ancientroleofsulfakinincholecystokinintypesignallingininhibitoryregulationoffeedingprocessesrevealedinanechinoderm
AT elizabethfgunner ancientroleofsulfakinincholecystokinintypesignallingininhibitoryregulationoffeedingprocessesrevealedinanechinoderm
AT cleidianegzampronio ancientroleofsulfakinincholecystokinintypesignallingininhibitoryregulationoffeedingprocessesrevealedinanechinoderm
AT alexandramjones ancientroleofsulfakinincholecystokinintypesignallingininhibitoryregulationoffeedingprocessesrevealedinanechinoderm
AT michaelaegertova ancientroleofsulfakinincholecystokinintypesignallingininhibitoryregulationoffeedingprocessesrevealedinanechinoderm
AT mauricerelphick ancientroleofsulfakinincholecystokinintypesignallingininhibitoryregulationoffeedingprocessesrevealedinanechinoderm
_version_ 1717761332468514816