Lyon College, Batesville, AR, United States.
Department of Biological Sciences, University of Arkansas, Fayetteville, AR, United States.
Front Endocrinol (Lausanne). 2020 Feb 19;11:63. doi: 10.3389/fendo.2020.00063. eCollection 2020.
Neuropeptides are ancient neuronal signaling molecules that have diversified across Cnidaria (e.g., jellyfish, corals, and sea anemones) and its sister group Bilateria (e.g., vertebrates, insects, and worms). Over the course of neuropeptide evolution emerged lineage-specific neuropeptides, but their roles in the evolution and diversification of nervous system function remain enigmatic. As a step toward filling in this knowledge gap, we investigated the expression pattern of a cnidarian-specific neuropeptide-RPamide-during the development of the starlet sea anemone , using hybridization and immunohistochemistry. We show that RPamide precursor transcripts first occur during gastrulation in scattered epithelial cells of the aboral ectoderm. These RPamide-positive epithelial cells exhibit a spindle-shaped, sensory-cell-like morphology, and extend basal neuronal processes that form a nerve net in the aboral ectoderm of the free-swimming planula larva. At the aboral end, RPamide-positive sensory cells become integrated into the developing apical organ that forms a bundle of long cilia referred to as the apical tuft. Later during planula development, RPamide expression becomes evident in sensory cells in the oral ectoderm of the body column and pharynx, and in the developing endodermal nervous system. At metamorphosis into a polyp, the RPamide-positive sensory nerve net in the aboral ectoderm degenerates by apoptosis, and RPamide expression begins in ectodermal sensory cells of growing oral tentacles. In addition, we find that the expression pattern of RPamide in planulae differs from that of conserved neuropeptides that are shared across Cnidaria and Bilateria, indicative of distinct functions. Our results not only provide the anatomical framework necessary to analyze the function of the cnidarian-specific neuropeptides in future studies, but also reveal previously unrecognized features of the sea anemone nervous system-the apical organ neurons of the planula larva, and metamorphosis-associated reorganization of the ectodermal nervous system.
神经肽是古老的神经元信号分子，在刺胞动物（如水母、珊瑚和海葵）及其姐妹群两侧对称动物（如脊椎动物、昆虫和蠕虫）中多样化。在神经肽进化过程中出现了谱系特异性神经肽，但它们在神经系统功能的进化和多样化中的作用仍然是个谜。为了填补这一知识空白，我们使用杂交和免疫组织化学技术，研究了一种刺胞动物特异性神经肽-RPamide 在明星海葵发育过程中的表达模式。我们发现，RPamide 前体转录物首先在原肠胚形成过程中在口后外胚层的分散上皮细胞中出现。这些 RPamide 阳性上皮细胞表现出纺锤形、感觉细胞样形态，并延伸出基底神经元突起，在自由游动的帽状幼虫的口后外胚层中形成神经网。在口端，RPamide 阳性感觉细胞整合到正在形成的顶端器官中，该器官形成一束称为顶端簇的长纤毛。在帽状幼虫发育后期，RPamide 在体柱和咽的口外胚层中的感觉细胞以及正在发育的内胚层神经系统中表达明显。在变态为水螅体时，口后外胚层中的 RPamide 阳性感觉神经网通过细胞凋亡退化，RPamide 表达开始于生长中的口触手的外胚层感觉细胞中。此外，我们发现 RPamide 在帽状幼虫中的表达模式与在刺胞动物和两侧对称动物中共享的保守神经肽不同，表明其具有独特的功能。我们的研究结果不仅提供了在未来研究中分析刺胞动物特异性神经肽功能所需的解剖框架，还揭示了海葵神经系统以前未被认识的特征，即帽状幼虫的顶端器官神经元和变态相关的外胚层神经系统重组。
