School of Biological & Chemical Sciences, Queen Mary University of London, Mile End Road, London, E1 4NS, UK.
Department of Clinical Neurosciences, MRC Cambridge Stem Cell Institute, University of Cambridge, Cambridge, CB2 0SZ, UK.
BMC Biol. 2019 Jul 31;17(1):60. doi: 10.1186/s12915-019-0680-2.
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.
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.
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.
血管加压素/催产素 (VP/OT)- 型神经肽作为利尿剂、生殖生理学和社会行为的调节剂而闻名。然而，我们对它们功能的了解主要基于脊椎动物和选定的原口动物无脊椎动物的研究结果。关于 VP/OT- 型神经肽在后口动物无脊椎动物中的作用知之甚少，后口动物与原口动物相比与脊椎动物更为密切相关。
在这里，我们鉴定并功能表征了一种 VP/OT- 型信号系统，该系统包括海星（星） Asterias rubens 中的神经肽 asterotocin 及其同源 G 蛋白偶联受体，海星是后生动物无脊椎动物，属于棘皮动物门。使用 mRNA 原位杂交和免疫组织化学分析 asterotocin 和 asterotocin 受体在 A. rubens 中的分布，发现其在中枢神经系统（辐射神经索和围口神经环）、消化系统（包括心脏胃）和体壁及其附属附属物中表达。根据 asterotocin 信号的解剖结构，体外药理学实验表明 asterotocin 作为海星的肌肉松弛剂，与 VP/OT- 型神经肽在脊椎动物中的肌肉作用相反。此外，体内注射 asterotocin 对海星行为产生了显著影响，引发了虚假摄食，其中心脏胃的外翻和身体姿势的变化类似于海星异常的口腔外摄食行为。
我们对棘皮动物中的 VP/OT- 型信号进行了全面表征，包括对 VP/OT- 型神经肽 asterotocin 和其同源受体的表达进行了详细的解剖分析。我们发现 asterotocin 触发海星的虚假摄食，为 VP/OT- 型神经肽作为动物摄食调节剂的古老作用提供了重要的新证据。
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