Ancient role of vasopressin/oxytocin-type neuropeptides as regulators of feeding revealed in an echinoderm

Autor: Abdullah K. Garewal, Michaela Egertová, Liisa M. Blowes, Radhika R. Patel, Dean C. Semmens, Jérôme Delroisse, Susan E. Slade, Esther A. Odekunle, Ana B. Tinoco, Meet Zandawala, James H. Scrivens, Nataly Martynyuk, Maurice R. Elphick
Přispěvatelé: Elphick, Maurice R [0000-0002-9169-0048], Apollo - University of Cambridge Repository
Rok vydání: 2020
Předmět:
Vasopressin
Physiology
Starfish
Central nervous system
Neuropeptide
Plant Science
Oxytocin
General Biochemistry
Genetics and Molecular Biology

03 medical and health sciences
0302 clinical medicine
Structural Biology
medicine
Animals
Amino Acid Sequence
Receptor
lcsh:QH301-705.5
Righting
Ecology
Evolution
Behavior and Systematics

Phylogeny
030304 developmental biology
0303 health sciences
Asterotocin
mRNA in situ hybridisation
biology
Echinoderm
Asterias
Feeding
Neuropeptides
Cell Biology
Feeding Behavior
biology.organism_classification
Immunohistochemistry
Cell biology
medicine.anatomical_structure
lcsh:Biology (General)
Cardiac stomach
Asterotocin receptor
General Agricultural and Biological Sciences
Sequence Alignment
030217 neurology & neurosurgery
Research Article
Developmental Biology
Biotechnology
medicine.drug
Zdroj: BMC Biology, Vol 17, Iss 1, Pp 1-23 (2019)
BMC Biology
DOI: 10.17863/cam.55688
Popis: Background Vasopressin/oxytocin (VP/OT)-type neuropeptides are well known for their roles as regulators of diuresis, reproductive physiology and social behaviour. However, our knowledge of their functions is largely based on findings from studies on vertebrates and selected protostomian invertebrates. Little is known about the roles of VP/OT-type neuropeptides in deuterostomian invertebrates, which are more closely related to vertebrates than protostomes. Results Here, we have identified and functionally characterised a VP/OT-type signalling system comprising the neuropeptide asterotocin and its cognate G-protein coupled receptor in the starfish (sea star) Asterias rubens, a deuterostomian invertebrate belonging to the phylum Echinodermata. Analysis of the distribution of asterotocin and the asterotocin receptor in A. rubens using mRNA in situ hybridisation and immunohistochemistry revealed expression in the central nervous system (radial nerve cords and circumoral nerve ring), the digestive system (including the cardiac stomach) and the body wall and associated appendages. Informed by the anatomy of asterotocin signalling, in vitro pharmacological experiments revealed that asterotocin acts as a muscle relaxant in starfish, contrasting with the myotropic actions of VP/OT-type neuropeptides in vertebrates. Furthermore, in vivo injection of asterotocin had a striking effect on starfish behaviour—triggering fictive feeding where eversion of the cardiac stomach and changes in body posture resemble the unusual extra-oral feeding behaviour of starfish. Conclusions We provide a comprehensive characterisation of VP/OT-type signalling in an echinoderm, including a detailed anatomical analysis of the expression of both the VP/OT-type neuropeptide asterotocin and its cognate receptor. Our discovery that asterotocin triggers fictive feeding in starfish provides important new evidence of an evolutionarily ancient role of VP/OT-type neuropeptides as regulators of feeding in animals. Electronic supplementary material The online version of this article (10.1186/s12915-019-0680-2) contains supplementary material, which is available to authorized users.
Databáze: OpenAIRE